Marine Microbiology by CB Munn

MARINE MICROBIOLOGY
The 3rd Edition of this book captures all the recent amazing advances in our understanding of the marine microbiology world
but still manages to present the concepts in a an easy, informative and entertaining way that will engage the novice to the expert.
What a great book and a fun read.
- David Bourne, James Cook University and The Australian Institute of Marine Science
It is great to see another edition of the book given that marine microbiology is such a fast moving and scientifically diverse field.
Munn’s new edition will be a great resource for new students and advanced scientists alike.
- Greta Reintjes, Max Planck Institute for Marine Microbiology, Bremen, Germany
Reading this textbook has made me realise how much the field of marine microbiology has progressed in recent decades.
I recommend this book also to biogeochemists and ecologists in search of the Big Picture of ocean functioning. The many details
of interactions emerging from the microbial world are amazing and shed light on the factors driving evolution of these ancient
ecosystems.
- Victor Smetacek, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
It has been astonishing to see the evolution of this book over the years. With its many ‘RESEARCH FOCUS’ boxes and
‘SIDEBARS’, this is more than your usual textbook. It is written in an enthusiastic, thought-provoking manner, encompassing
the most up-to-date concepts in marine microbiology. From planktonic tunicates involved in carbon cycling, to viruses infecting
other viruses, this essential read has it all!
- Jozef I. Nissimov, Lecturer in Microbial Oceanography, SAMS, Scottish Marine Institute, UK
Colin B. Munn obtained a BSc (Hons) degree from University College London and a PhD from the University of Birmingham. He
is an Honorary Fellow of the Marine Institute of University of Plymouth, England and was Associate Professor of Microbiology
and Admissions Tutor for Marine Biology programs until 2017. He has a long experience of research in various aspects of
microbiology, with particular interests in the interactions between symbiotic and pathogenic microorganisms and their hosts.
He has held former positions as Visiting Professor at the University of Victoria, Central University of Venezuela and St Georges
University, Grenada and a visiting researcher (Leverhulme Fellow) at James Cook University and the Australian Institute of
Marine Science. He has served as external examiner for Bachelor’s, Master’s, and PhD degrees in many countries and as a special
assessor for molecular and organismal biology for the UK Quality Assurance Agency for Higher Education. He has extensive
research experience in a range of microbiological topics, with special interest in interactions between pathogenic and symbiotic
microbes and their hosts.
MARINE MICROBIOLOGY
ECOLOGY & APPLICATIONS

Third Edition
Colin B. Munn
CRC Press
Taylor & Francis Group
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Contents
Chapter 1 Microbes in the Marine Microbes in sea ice form an important part of the food
web in polar regions 22
Environment 1 Microbial activity underpins productive food webs in
ORIGINS AND SCOPE OF MARINE coral reefs 25
MICROBIOLOGY 2 Living organisms are the habitats of many microbes 25
Conclusions 25
Marine microbiology has developed into one of the most References and further reading 26
important areas of modern science 2
Microbes include microscopic cellular organisms and
non-cellular viruses 2 Chapter 2 Methods in Marine
Marine microorganisms are found in all three domains of Microbiology 29
cellular life 3
Horizontal gene transfer confounds our understanding of SAMPLING METHODS 30
evolution 4 Sampling the marine environment requires special
Viruses are non-cellular entities with great importance in techniques 30
marine ecosystems 4
Microbial processes shape the living world 5 IMAGING TECHNIQUES 32
Marine microbes show great variation in size 5 Light and electron microscopy are used to study
OCEAN HABITATS 6 morphology and structure of microbes 32
Epifluorescence light microscopy enables enumeration
The world’s oceans and seas form an interconnected of marine microbes 33
water system 6 Confocal laser scanning microscopy enables recognition
The upper surface of the ocean is in constant motion of living microbes within their habitat 35
owing to winds 8 Flow cytometry measures the number and
Deep-water circulation systems transport water between size of particles 35
the ocean basins 8 Fluorescent in situ hybridization (FISH) allows
Light and temperature have important effects on visualization and quantification of specific microbes 36
microbial processes 9
Microbes occur in all the varied habitats found in CULTIVATION OF MICROORGANISMS 38
the oceans 10 Different microorganisms require specific culture media
Seawater is a complex mixture of inorganic and organic and conditions for growth 38
compounds, colloids, and gels 10 Enrichment culture selects for microbes with specific
The sea surface is covered by a gelatinous biofilm 14 growth requirements 40
SEDIMENTS AND SURFACES 14 Phenotypic testing is used for characterization of many
cultured bacteria 40
Microbes play a major role in marine sediments 14 Analysis of microbial cell components can be used for
Deep marine sediments contain a vast reservoir of bacterial classification and identification 42
ancient microbes 16
Microbes colonize surfaces through formation of METHODS BASED ON DNA AND RNA ANALYSIS 42
biofilms and mats 16 Nucleic acid-based methods have transformed
SOME EXAMPLES OF SPECIAL HABITATS—THE understanding of marine microbial diversity
DEEP SEA, POLAR OCEANS, CORAL REEFS, AND and ecology 42
LIVING ORGANISMS 19 Amplification and sequencing of ribosomal RNA
genes is widely used in microbial systematics and
Microbial activity at hydrothermal vents fuels an oasis diversity studies 42
of life in the deep sea 19 Isolation of genomic DNA or RNA is the first step in all
Cold seeps also support diverse life based on nucleic acid-based investigations 45
chemosynthesis 21 The polymerase chain reaction (PCR) forms the basis of
Microbes inhabit the interface of brine pools in the deep sea 21 many techniques 45
vi CONTENTS
Genomic fingerprinting can be used to assess diversity

SOURCES OF ENERGY AND CARBON 73
of cultured isolates 47
Microbes obtain energy from light or oxidation of

Determination of DNA properties is used in bacterial
compounds 73
and archaeal taxonomy 48
Microbes differ in their source of carbon to make
DNA sequence data are used for identification and
cellular material 74
phylogenetic analysis 48
DGGE and TRFLP can be used to assess composition

PHOTOTROPHY AND CHEMOTROPHY 74
of microbial communities 49
Phototrophy involves conversion of light energy to
Advances in DNA sequencing enable improved microbial
chemical energy 74
community analysis 50
Oxygenic photosynthesis involves two distinct but
Elucidating the full genome sequence of microbes

coupled photosystems 76
provides insights into their functional roles 52

Anaerobic anoxygenic photosynthesis uses only one
Metabarcoding and metagenomics have led to major

type of reaction center 76
advances in microbial community analysis 53

Aerobic anoxygenic phototrophy is widespread in
Omics technologies provide information about the

planktonic bacteria 77
functional gene composition of a microbial community 55

Some phototrophs use rhodopsins as light-harvesting
Genomes can now be obtained from single cells in

pigments 77
environmental samples 56
Chemolithotrophs use inorganic electron donors as
IN SITU ACTIVITY OF MICROBIAL COMMUNITIES 57

a source of energy and reducing power 79
Many bacteria oxidize sulfur compounds 80
Microelectrodes and biosensors measure microbial
Many chemolithotrophs use hydrogen as an
processes at the microhabitat scale 57
electron donor 81
Radioisotopes can be used to detect metabolic activity
Bacterial and archaeal nitrification is a major process
in a community 57
in the marine nitrogen cycle 81
Stable-isotope probing (SIP) tracks fluxes of nutrients in
Ammonia can also support anaerobic
communities 58
chemolithoautotrophy 82
NanoSIMS allows metabolic transfers to be measured at
subcellular levels 58
CARBON AND NITROGEN FIXATION 83
Microarrays enable assessment of gene activity in the

The Calvin–Benson–Bassham (CBB) cycle is the main
environment 59
method of carbon fixation in autotrophs 83
Metatranscriptomics, metaproteomics, and metabolomics

Some Archaea and Bacteria use alternative pathways
reveal microbial activities in the environment 59

to fix CO2 83
Microfluidics enables study of microscale processes 60

Fixation of nitrogen makes this essential element
Mesocosm experiments attempt to simulate natural

available for building cellular material in all life 84
conditions 60
Remote sensing permits global analysis of microbial

HETEROTROPHIC METABOLISM 85
activities 61
Many marine microbes obtain energy by the
Conclusions 62
fermentation of organic compounds 85
References and further reading 62

Anaerobic respiration has major importance in marine
processes 86
Chapter 3 Metabolic Diversity and

Nitrate reduction and denitrification release nitrogen and
other gases 86
Ecophysiology 65
Sulfate reduction is a major process in marine sediments 86
A BRIEF OVERVIEW OF CELL STRUCTURE AND

MICROBIAL PRODUCTION AND OXIDATION OF
FUNCTION 66
METHANE 87
Bacteria and archaea show a variety of cell forms and

Methanogenesis is unique to the Archaea 87
structural features 66
Methane is produced in the surface ocean by bacterial
The cytoplasmic membrane controls cell processes via

cleavage of phosphonates 88
transport of ions and molecules 66

Anaerobic oxidation of methane (AOM) in sediments is
Cells may contain organelles, microcompartments, and

coupled to sulfate reduction 88
inclusion bodies 67
Many marine microbes oxidize methane and other C1
The nature of the cell envelope has a major effect on

compounds 90
physiology 68
NUTRIENT ACQUISITION AND MICROBIAL
Genome size and organization determines bacterial and

GROWTH 90
archaeal lifestyles 69
Microbes use a variety of mechanisms to regulate

Microbial metabolism depends on nutrient uptake 90
cellular activities 73
CONTENTS vii
Acquisition of iron is a major challenge for marine The order Caulobacterales contains prosthecate bacteria 121
microbes 92
Several alphaproteobacterial genera show magnetotaxis 123
Marine bacterioplankton use two trophic strategies 92

Magnetotaxis is also found in other classes and phyla 124
Growth rate and turnover of organic material depend on

The order Betaproteobacteriales includes many
nutrient concentrations 93
rare OTUs 124
Copiotrophic marine bacteria may show rapid growth

The Gammaproteobacteria is a very large and
in culture 93
diverse class 124
Bacteria adapt to starvation by coordinated changes to

The Gammaproteobacteria includes many uncultivated
cell metabolism 94
species of sulfide-oxidizing bacteria (SOB) 126
Some bacteria enter a “viable but nonculturable” state

The family Vibrionaceae includes many important
in the environment 95
pathogens and symbionts 127
Many bacteria use motility to search for nutrients and

Members of the order Oceanospirillales break down
optimal conditions 95
complex organic compounds 127
Flagella also have a mechanosensory function 97

The family Thiotrichaceae includes some
Microbes also respond to light, magnetic fields, and

important SOB 128
other stimuli 100

The proposed phylum Desulfobacterota contains
Gliding and twitching motility occur on surfaces 100

anaerobic sulfate- or sulfur-reducing bacteria (SRB) 129
Microbes colonize surfaces via formation of biofilms 101

The proposed phylum Epsilonbactereota contains major
Pili are important for bacterial attachment to surfaces

contributors to productivity at hydrothermal vents 129
and genetic exchange 102

Myxobacteria have a complex life cycle 132
Antagonistic interactions between microbes occur on

The Bdellovibrionales contains predatory bacteria 132
particles or surfaces 102

Members of the Zetaproteobacteria are microaerophilic
Quorum sensing is an intercellular communication

iron-oxidizers 133
system for regulation of gene expression 102

Members of the Cyanobacteria carry out oxygenic
PHYSICAL EFFECTS ON MICROBIAL GROWTH

photosynthesis 133
A genome-based classification of the Cyanobacteria is
AND SURVIVAL 105
under development 134
Most marine microbes grow at low temperatures 105

Prochlorococcus is the most abundant photosynthetic
Microbes growing in hydrothermal systems are

organism 134
adapted to very high temperatures 105

Synechococcus spp. dominate the upper photic zone 136
Microbes that inhabit the deep ocean must withstand

Some free-living and symbiotic cyanobacteria
a very high hydrostatic pressure 106

fix nitrogen 136
Ultraviolet irradiation has lethal and mutagenic effects 107

Filamentous cyanobacteria are important in the
Bacterial bioluminescence may protect bacteria from

formation of microbial mats 139
ROS and UV damage 108

Members of the Planctomycetes have atypical cell
Microbes use various mechanisms to prevent

structure 139
osmotic damage 108

The phylum Bacteroidetes has a major role in nutrient
Conclusions 109
cycling via degradation of polymers 140

Members of the phylum Chloroflexi are widespread but
poorly characterized 141
Chapter 4 Diversity of Marine

The phyla Aquificae and Thermotogae are deeply
Bacteria 113
branching primitive thermophiles 141
The Firmicutes are a major branch of Gram-
OVERVIEW OF BACTERIAL DIVERSITY 114

positive Bacteria 142
Members of the Actinobacteria are a rich source of
Understanding of diversity has been revolutionized by secondary metabolites, including antibiotics 143
phylogenetic and genomic techniques 114

Conclusions 144
Bacterial systematics is in transition due to application

of genomic methods 115
OTUs and ASVs are used to represent diversity in
community analyses 118

Chapter 5 Marine Archaea 149
Marine microbial communities show high alpha

Several aspects of cell structure and function
diversity 119
distinguish the Archaea and Bacteria 150
A TOUR OF THE BACTERIAL AQUARIUM 120

New phylogenomic methods have led to recognition of
multiple phyla of the Archaea 150
The Proteobacteria account for about half of all

bacterial ocean diversity 121
PHYLUM EURYARCHAEOTA 151
Members of the class Alphaproteobacteria are the most

Many members of the Euryarchaeota produce methane 151
abundant marine bacteria 121
viii CONTENTS
Anaerobic oxidation of methane (AOM) in sediments is Photosynthetic prasinophytes are abundant members
carried out by syntrophic archaea 153 of the picoplankton 184
The class Thermococci contains hyperthermophiles Amoebozoa are important grazers of particle-
found at hydrothermal vents 154 associated bacteria 184
Archaeoglobus and Ferroglobus are hyperthermophilic Radiolarians and foraminifera have highly diverse
sulfate-reducers and iron-oxidizers 155 morphologies with mineral shells 185
The Euryarchaeota contains extreme halophiles 155 MARINE FUNGI 186
Uncultivated members of the Euryarchaeota are
abundant in the plankton 155 The Fungi form a distinct monophyletic group on a
branch within the Nucletmycea 186
PHYLUM CRENARCHAEOTA 156
Fungi are increasingly recognized to be major
Members of the Crenarchaeota are thermophiles components of the marine microbiome 187
occurring in hydrothermal vents 156 Conclusions 189
PHYLUM THAUMARCHAEOTA 157 References and further reading 192
A single clade of ammonia-oxidizing archaea

comprises 20% of the picoplankton 157 Chapter 7 Marine Viruses 195
PHYLUM NANOARCHAEOTA 161 Viruses are highly diverse non-cellular microbes 196
Phages are viruses that infect bacterial and
Nanoarchaeum is an obligate parasite of another archaeal cells 200
archaeon 161 The life cycle of phages shows a number of
Conclusions 162 distinct stages 201
References and further reading 162 Lysogeny occurs when the phage genome is integrated
into the host genome 201
Chapter 6 Marine Eukaryotic Loss of viral infectivity arises from damage to the
nucleic acid or capsid 205
Microbes 165 Measurement of virus production rates is important for
quantifying virus-induced mortality 205
MARINE PROTISTS 166
Viral mortality “lubricates” the biological pump 206
Protists are a highly diverse collection of unicellular Nucleocytoplasmic large DNA viruses (NCLDVs) are
eukaryotic microbes 166 important pathogens of microalgae and other protists 206
Protists show enormous diversity and classification Other giant viruses are abundant pathogens of
systems are regularly revised 167 heterotrophic protists 210
The -omics approaches have some limitations for RNA viruses also infect protists 211
understanding protist diversity 168 Viral mortality plays a major role in structuring
Picoeukaryotes play a major role in ocean food webs 169 diversity of microbial communities 212
Heterotrophic flagellated protists play a major role in Marine viruses show enormous genetic diversity 214
grazing of other microbes 169 Viromes are creators of genetic diversity and exchange 215
Heterotrophic flagellated protists have different feeding Conclusions 215
mechanisms 170 References and further reading 215
Many protists are mixotrophic 172
The choanoflagellates have a unique morphology
Chapter 8 Microbes in Ocean
and feeding mechanism 172
Dinoflagellates have several critical roles in Processes—Carbon Cycling 219
marine systems 173 Physical factors and biotic processes determine the
Dinoflagellates and other protists undertake diel fate of carbon in the oceans 221
vertical migration 175 Marine phytoplankton are responsible for about half
Some dinoflagellates exhibit bioluminescence 176 of the global primary production 222
The ciliates are voracious grazers of other protists There are wide geographical and seasonal variations in
and bacteria 177 primary production 224
The haptophytes (prymnesiophytes) are some of the Dark ocean carbon fixation makes a major contribution
most abundant components of ocean phytoplankton 178 to primary production 226
Diatoms are extremely diverse and abundant primary Classic food chain and microbial loop processes occur
producers in the oceans 181 in the epipelagic 226
Other stramenopiles may cause harmful blooms 183 The microbial loop results in retention of dissolved
Thraustochytrids and labyrinthulids are active nutrients 227
degraders of organic matter 183 The biological pump transports fixed carbon to the
deep ocean and sediments 228
CONTENTS ix
Carbon export of primary production may change due THE SILICON CYCLE 253
to ocean warming and acidification 228
Silicification of diatoms is an economic process for
Ingestion of bacteria by protists plays a key role in the
construction of a cell wall 253
microbial loop 229
Diatom blooms depend on the availability of silica
The viral shunt catalyzes nutrient regeneration in the
in the environment 254
upper ocean 230
Eutrophication alters the silicon balance in
Microbial processes alter the composition of DOM 231
coastal zones 254
Eutrophication of coastal waters stimulates
Conclusions 255
microbial activity 232
Conclusions 233
Chapter 10 Microbial Symbioses of
Chapter 9 Microbes in Ocean Marine Animals 259
Processes—Nitrogen, Sulfur, Iron, Symbioses occur in many forms 260
Phosphorus, and Silicon Cycling 235 Chemosynthetic bacterial endosymbionts of animals
were discovered at hydrothermal vents 260
NUTRIENT LIMITATION 236 A wide range of other chemosynthetic endosymbioses
occurs in the deep sea 264
Key elements act as limiting nutrients for Chemosynthetic symbioses are also widespread in
phytoplankton 236 shallow-water sediments 266
Productivity of surface waters shows marked Animals colonizing whale falls depend on autotrophic
geographical variations 236 and heterotrophic symbionts 269
Ocean microbes require iron 237 Sea squirts harbor photosynthetic bacteria 269
Terrestrial runoff, dust, and volcanic ash are major Endosymbionts of bryozoans produce compounds that
sources of iron input 237 protect the host from predation 270
Hydrothermal vents and glacial melting also supply Sponges contain dense communities of specific microbes 273
iron to the oceans 238 Many marine invertebrates depend on photosynthetic
Whales and seabirds play a major role in supply of endosymbionts 275
iron to phytoplankton 241 Zooxanthellae (Symbiodiniaceae) show extensive
THE NITROGEN CYCLE 241 genetic diversity and host specificity 275
Many corals are dependent on zooxanthellae for nutrition 276
There have been major shifts in our understanding
Coral bleaching occurs when the host–symbiont
of the marine nitrogen cycle 241
interactions are uncoupled 278
Diazotrophs incorporate atmospheric nitrogen into
The coral holobiont contains multiple microbial partners 280
organic material 241
Zooxanthellae boost the growth of giant clams 281
Fixed nitrogen is returned to the inorganic pool by
Some fish and invertebrates employ symbiotic bacteria
ammonification and nitrification 243
to make light 284
Assimilation of ammonium and nitrate fuels growth
The bobtail squid uses bacterial bioluminescence for
of phytoplankton and other microbes 244
camouflage 286
Nitrate reduction, denitrification, and anammox reactions
Conclusions 287
return nitrogen to its elemental form and other gases 244
Diverse microbial metabolic processes occur in oxygen
minimum zones (OMZs) 245
Microbial processes in sediments are a major Chapter 11 Microbial Diseases of
contributor to nitrogen cycling 247 Marine Organisms 291
THE SULFUR CYCLE 247 Diseases of marine organisms have major ecological
The oceans and sediments contain large quantities and economic impact 292
of sulfur compounds 247 DISEASES OF CORALS, SPONGES,
Metabolism of organic sulfur compounds is especially AND ECHINODERMS 292
important in surface waters 248

DMSP production leads to release of the climate-active Infectious diseases threaten the survival of corals 292
gas dimethyl sulfide (DMS) 248 Vibrios are associated with many coral diseases 293
The fungus Aspergillus sydowii caused mass mortality
THE PHOSPHORUS CYCLE 252 of sea fans in the Caribbean Sea 295
Phosphorus is often a limiting or co-limiting nutrient 252 Black band disease of corals is a disease of corals
Marine microbes are adapted to low and variable worldwide 295
levels of phosphorus 252
x CONTENTS
White plague and white pox are major diseases DISEASES OF MAMMALS 320
affecting Caribbean reefs 298
Dinoflagellate and diatom toxins affect
Protistan parasites may cause tissue necrosis and
marine mammals 320
skeletal erosion 299
Virus disease cause mass mortalities in cetaceans and
Viruses have a pivotal role in coral health 300
pinnipeds 321
Sponge disease is a poorly investigated global
Viruses from nine different families have been linked
phenomenon 301
to diseases of marine mammals 321
Mass mortalities of echinoderms have caused major
Several species of bacteria and fungi infect marine
shifts in reef and coastal ecology 303
mammals 323
DISEASES OF MOLLUSCS 304
DISEASES OF SEA TURTLES 323
Bacteria are a major cause of disease in molluscs 304
Sea turtles are affected by a virus promoting growth
Several protistan diseases affect culture of oysters
of tumors 323
and mussels 305
Virus infections are a major problem in oyster culture 306 DISEASES OF SEAGRASSES AND SEAWEEDS 324
DISEASES OF CRUSTACEANS 306 Heterokont protists cause ecologically important
mortality of seagrasses 324
Bacteria cause epizootics with high mortalities in
Bacteria, fungi, and viruses infect marine macroalgae 324
crustaceans 306
Conclusions 326
Expansion of crustacean aquaculture is threatened by
viral diseases 307
Parasitic dinoflagellates also cause
disease in crustaceans 309 Chapter 12 Marine Microbes as
DISEASES OF FISH 309 Agents of Human Disease 331
Microbial diseases of fish cause major losses in
MICROBIAL INFECTIONS 332
aquaculture and natural populations 309
Microbial infections of fish cause a variety of Pathogenic vibrios are common in marine and
disease signs 310 estuarine environments 332
Fish-pathogenic bacteria possess a range of virulence Vibrio cholerae is an autochthonous aquatic bacterium 332
mechanisms 311 Complex regulatory networks control human
Vibrios are responsible for some of the main infections colonization and virulence of V. cholerae 333
of marine fish 311 Mobile genetic elements play a major role in the
Pasteurellosis affects warm-water marine fish 313 biology of Vibrio spp. 333
Aeromonas salmonicida has a broad geographic range Non-O1 and non-O139 serotypes of Vibrio cholerae are
affecting fish in fresh and marine waters 314 widely distributed in coastal and estuarine waters 335
Marine flexibacteriosis is caused by a weakly virulent Vibrio vulnificus is a deadly opportunistic pathogen 337
opportunist pathogen 315 Pathogenicity of V. vulnificus is due to the interaction
Piscirickettsia and Francisella are intracellular of multiple gene products 338
proteobacteria infecting salmon and cod 316 Environmental factors affect the pathogenicity of
Intracellular Gram-positive bacteria cause chronic V. vulnificus 338
infections of fish 316 Vibrio parahaemolyticus is the leading cause of
Some Gram-positive cocci affect the central nervous seafood-associated gastroenteritis 339
system of fish 317 Microbes associated with fish and marine mammals
Viruses cause numerous diseases of marine fish 318 can be transmitted to humans 340
Infectious salmon anemia (ISA) is one of the most DISEASES CAUSED BY MARINE MICROBIAL
serious diseases in salmon culture 318 TOXINS 341
Viral hemorrhagic septicemia (VHS) virus infects many
species of wild fish 318 Scombroid fish poisoning results from bacterial
Lymphocystis virus causes chronic skin infection of fish 319 enzyme activity 341
Birnaviruses appear to be widespread in marine fish Botulism is a rare lethal intoxication from seafood 341
and invertebrates 319 Fugu poisoning is caused by a neurotoxin of
Viral nervous necrosis (VNN) is an emerging disease bacterial origin 342
with major impact 319 TTX is widespread amongst marine animals 343
Protists cause disease in fish via infections, toxins, Some dinoflagellates and diatoms produce harmful
and direct physical effects 319 toxins 343
CONTENTS xi
Paralytic shellfish poisoning is caused by saxitoxins Shellfish from sewage-polluted waters can cause
produced by dinoflagellates 344 human infection 369
Brevetoxin causes illness via ingestion or inhalation Microbiological standards are used for classification of
during red tides 346 shellfish production areas 370
Dinophysiotoxins and azaspiracid toxins from shellfish Direct testing for pathogens in shellfish is possible with
result in gastrointestinal symptoms 346 molecular methods 371
Amnesic shellfish poisoning is caused by toxic diatoms 347 OIL AND OTHER CHEMICAL POLLUTION 372
Ciguatera fish poisoning has a major impact on the
health of tropical islanders 347 Oil pollution of the marine environment is a
Bacteria influence the production of HAB toxins 349 major problem 372
Dinoflagellate and diatom toxins may be antipredator Microbes naturally degrade oil in the sea 372
defense mechanisms 349 Physical and biological processes affect the fate
Complex factors affect the incidence of HABs and of oil spills 373
toxin-associated diseases 350 Bioremediation of oil spills may be enhanced by
Coastal waters must be regularly monitored to assess emulsifiers and nutrients 373
the development of HABs 351 Microbes can detoxify heavy metals from contaminated
Conclusions 351 sediments 376
References and further reading 352 Microbial systems can be used for
ecotoxicological testing 377
Microbial adsorption and metabolism affect
Chapter 13 Microbial Aspects of accumulation of mercury 377
Marine Biofouling, Biodeterioration, Microbial cycling is important in the distribution of
persistent organic pollutants 377
and Pollution 355 Plastic pollution of the oceans is a major global problem 378
Conclusions 379
BIOFOULING AND BIODETERIORATION 356 References and further reading 382
Microbial biofilms initiate the process of biofouling 356
Microbes induce corrosion of metals, alloys, and
composite materials 357
Chapter 14 Marine Microbial
Microbes cause biodeterioration of timber and marine Biotechnology 387
wooden structures 358 Enzymes From Marine Microbes Have Many
Microbial growth and metabolism cause spoilage of Applications 388
seafood products 359 DNA polymerases from hydrothermal vent organisms
Processing, packaging, and inhibitors of spoilage are are widely used in molecular biology 390
used to extend shelf-life 360 Metagenomics and bioinformatics lead to new
Some seafood products are made by deliberate biotechnological developments 390
manipulation of microbial activities 361 Polymers from marine bacteria have many applications 391
MARINE POLLUTION BY SEWAGE AND Microalgae can produce biofuels and edible oils 391
WASTEWATER 361 Marine microbes are a rich source of biomedical
products393
Coastal pollution by wastewater is a source of
Many bioactive compounds from marine invertebrates are
human disease 361
produced by microbes 393
Human viral pathogens occur in sewage-
With so much potential from the sea, why are there so
polluted seawater 362
few new drugs? 395
Fecal indicator organisms (FIOs) are used to assess
Study of complex microbial communities may lead to
public health risks 363
new antibiotics 395
Coliforms and E. coli are unreliable FIOs for seawater
Marine microbes provide various health-
monitoring 363
promoting products 396
Enterococci are more reliable FIOs for seawater
Marine microbes have applications in biomimetics,
monitoring 364
nanotechnology, and bioelectronics 396
Molecular-based methods permit quicker analysis of
Microbial biotechnology has many applications in
indicator organisms and microbial source tracking 365
aquaculture 397
Various alternative indicator species have been
Antimicrobial agents are widely used in aquaculture 397
investigated 366
Antimicrobial resistance (AMR) is a major problem in
Countries have different quality standards for
aquaculture 399
bathing waters 367
Vaccination of finfish is widely used in aquaculture 400
xii CONTENTS
Recombinant DNA technology is used to produce Conclusions 405

vaccines for diseases caused by viruses and References and further reading 406
some bacteria 401
Live attenuated vaccines are effective but not
widely used 402 Chapter 15 Concluding Remarks 409
DNA vaccination depends on fish cells expressing a
protective antigen 402
Probiotics, prebiotics, and immunostimulants are
widely used in aquaculture 403 Index 411
List of Research Focus Boxes
1.1 Deep subsurface microbes—are they dead,

9.1 Can artificial fertilization of the oceans with iron
dormant, or just staying alive?

help to mitigate global warming?
1.2 What will happen when the sea-ice melts?

9.2 Transformations of DMSP are major drivers of
diverse ocean processes
2.1 Cultivating the uncultured
10.1 Genomic insights into host–symbiont
3.1 Microbes use solar power to top up energy levels
interactions: infection, colonization, and dissemination
3.2 How can microscale bacterial swimming affect
10.2 Chemosynthetic bacteria fuel ecosystem-
global processes?
engineering bivalves
4.1 High-throughput DNA sequencing provides new
10.3 Do corals have a core microbiome?
insights into marine microbial diversity
10.4 Genomic insights into the evolution of
4.2 Cable bacteria unite to conduct electricity
bioluminescent symbionts of fish
5.1 Evolution of an evolutionary pathway—changing
11.1 The pathogenicity of Vibrio coralliilyticus
views of Archaea in the tree of life
11.2 Caribbean corals under threat from a new
5.2 Deep-sea FISHing—discovery of the role of
disease syndrome
archaea in carbon and nitrogen cycling
12.1 Are human Vibrio infections a microbial
6.1 Sailing towards a better understanding of
barometer for climate change?
heterotrophic ocean protists
13.1 Is it safe to swim? The health effects of
6.2 Exciting times for marine mycology
recreational exposure to seawater
7.1 Models for the co-evolution of bacteria and their phages
13.2 How microbes cleaned up deep-sea oil after the
7.2 “Bloom and bust”—the life cycle of Emiliania

Deepwater Horizon (DWH) disaster
huxleyi and Coccolithovirus (EhV)

13.3 Microorganisms and microplastics
7.3 New ideas about the nature and evolution of viruses
14.1 “The enemy of my enemy is my friend”—phage
8.1 The role of microbes in the ocean carbon cycle

therapy for marine diseases
Preface
In the Foreword to the Second Edition of this textbook published in 2011, Farooq Azam,
Distinguished Professor of Scripps Institution of Oceanography, wrote:
When we think of the ocean we might think of whales, waves, dolphins, fish, the smell of
the sea, its blue color, and its vastness; most of us would not look out at the sea and think
of marine microbes, nor did marine scientists for over a century. They sailed the seas and
strenuously dragged plankton nets through the ocean’s pelagic zone to capture what they
judged would represent the marine biota. But they were unaware that the great majority of
the biota, perhaps 99 percent, easily streamed through the holes of their nets; the holes were
simply too big to capture these microbes. Even when membrane filters and microscopy
were used, and they revealed great diversity of microplankton and nanoplankton, most
microbes evaded detection. The view of the pelagic web of life that emerged, and became
entrenched for a century, was then based on a tiny fraction of marine biota. As a result, fish
eries scientists used models that did not include marine microbes, as did marine chemists
and geochemists who studied how biological forces influenced the grand cycles of elements
in the ocean. Much had to be revised as the major roles of the microbes were discovered,
following the development of new concepts, incisive imaging, and molecular methods to
observe and study marine plankton.
In this Third Edition, it will become clear that astonishing advances in marine microbiology
have continued to propel the discipline to be one of the most important areas of modern sci
ence. I hope that readers will share a sense of my excitement of learning about new discover
ies in this fascinating and fast-moving subject.
This book is intended primarily for upper-level undergraduates and graduate students, but
I anticipate that it will also prove useful to researchers who are interested in some of the
broader aspects and applications outside of their specific area of investigation. University
courses often include some element of microbiology as a specialist option for oceanography
or marine biology majors who have little previous knowledge of microbiology, but marine
microbiology is lightly covered in most textbooks. I hope that this book may play some part
in rectifying this deficiency. I also hope that the book will be useful to microbiology majors
studying courses in environmental microbiology, who may have little knowledge about ocean
processes or the applications of the study of marine microorganisms. I have attempted to
make the book sufficiently self-contained to satisfy all of the various potential audiences.
Above all, I wanted to create a book that is enjoyable to read, with the overall aim of bring
ing together an understanding of microbial biology and ecology with consideration of the
applications for environmental management, human welfare, health, and economic activity.
As will become evident, many common themes and recurring concepts link the activities,
diversity, ecology, and applications of marine microbes. In each chapter, I have attempted to
summarize the current state of knowledge about each aspect, with extensive cross-linking to
other sections. To improve readability, I rarely cite specific references in the main text, but
each chapter contains special interest boxes, which contain references to recent research.
Short boxes marked with the symbols or highlight important questions or interest
ing facts that supplement the main text. The choice of these topics is entirely my personal
whim—they represent subjects that I think are particularly intriguing, exciting, controver
sial, or sometimes fun. Each chapter contains one to three Research Focus Boxes—these are
intended to be relatively self-contained “mini-essays,” which explore in more detail some
hot topics of investigation. Examples include the impacts of rising CO2 levels on microbial
community structure and ocean processes, interactions of microbes with plastic pollution,
symbiotic interactions, and emerging diseases of marine life. They are not intended to be
exhaustive reviews, but I hope that they serve as a stimulus for students to follow up some of
the original research papers suggested and use these as a starting point for further inquiry or
xvi PREFACE
discussion in seminars. The reference list for each chapter contain numerous suggestions for
further reading.
The great advances in marine microbiology have occurred because of the development and
application of innovative new techniques. Therefore, an understanding of the main principles
of these methods is essential if the student is to make sense of research findings. Chapter 2
is written in a style that concentrates on the principles and avoids too much technical detail,
so I implore you to read this chapter right through at an early stage to gain an overview of
methods, referring back whenever a particular technique is mentioned later.
What’s new in this edition? The general aims and structure of the book are similar, but all
material has been updated and most sections have been completely rewritten and expanded to
take account of the many new discoveries in this field since the second edition was published
in 2011, especially the astonishing advances due to extensive application of high-through
put sequencing, single cell genomics, and analysis of large datasets. Significant advances in
understanding the diversity and evolution of bacteria, archaea, fungi, protists, and viruses
are discussed and their importance in marine processes is explored in detail. There are many
new color diagrams, illustrations, and boxes to aid students’ interest and understanding. I
have also tried to incorporate the numerous helpful comments received from students, course
leaders, and reviewers about previous editions and early drafts of this one. In addition, the
book has a companion website, which provides additional online resources for instructors
and students, including a summary of key concepts and terminology for each chapter, links
to further resources, artwork, videos, and more. My personal blog at www.marinemicro.org
also contains news and longer research articles.
Despite an exhaustive review process, astute readers will undoubtedly spot some errors and
omissions, or have suggestions for improvement. I welcome your comments—please e-mail
me at [email protected] or via the publishers.
Acknowledgments
This book would not have been possible without the continued stimulation of ideas through
teaching my university courses and mentoring research students. It has been a source of
immense pleasure and pride to see my efforts come full circle through the authoritative input
of several of my former students who have gone on to establish successful research careers
in marine microbiology. I am indebted to them and to the many other scientific colleagues
listed below, who gave up their time to comment on the original proposal, review drafts, and
provide valuable suggestions to improve the text. I also thank all those colleagues who pro
vided images, especially Davis Laundon for his spectacular cover design. I am particularly
grateful to Alice Oven, Senior Editor at CRC Press, for her enthusiasm and encouragement
to produce a Third Edition and for developing the new improved design for the book. I also
thank Sadé Lee, Damanpreet Kaur, Andrew Corrigan, and other members of the editorial
and design team at CRC Press for their expertise and help. Finally, to Sheila—thank you for
your constant love, support, and patience during this venture.
Colin B. Munn,
Marine Institute,
University of Plymouth, UK.
Reviewers
Mike Allen, University of Exeter and Plymouth Marine Laboratory; Rudolf Amann, Max
Planck Institute for Marine Microbiology; Craig Baker-Austin, CEFAS Laboratory; David
Bourne, AIMS and James Cook University; Mya Breitbart, University of South Florida;
Craig Carlson, University of California, Santa Barbara; Ian Cooper, University of Brighton;
Michael Cunliffe, Marine Biological Association of the UK; Jesse Dillon, California
State University, Long Beach; Stuart Donachie, University of Hawaii, Manoa; Alexander
Gruhl, Max Planck Institute for Marine Microbiology; Marcelo Gutiérrez, Universidad de
Concepción, Chile; Oliver Jäckle, Max Planck Institute for Marine Microbiology; Christina
Kellogg, US Geological Survey, St. Petersburg Coastal and Marine Science Center; Anne
Leonard, University of Exeter; Davis Laundon; Marine Biological Association of the UK;
Sophie Leterme, Flinders University; Lauren Messer, University of Queensland; Jozef
Nissimov, Scottish Association for Marine Science; Mircea Podar, Oak Ridge National
Laboratory; Elizabeth Robertson, Gothenburg University; Emma Ransome, Imperial
College London; Greta Reintjes, Max Planck Institute for Marine Microbiology; Wolfgang
Sand, University of Duisberg-Essen; Val Smith, University of St Andrews; Victor Smetacek,
Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research; Roman Stocker,
Environmental Microfluidics Group, ETH Zürich; Ben Temperton, Exeter University;
Jack Thomson, University of Liverpool; Malin Tietjen, Max Planck Institute for Marine
Microbiology; Richard Thompson, University of Plymouth; Rebecca Vega-Thurber, Oregon
State University; Jack Wang, University of Queensland; Joanna Warwick-Dugdale, Plymouth
Marine Laboratory and University of Exeter; Robyn Wright, University of Warwick; Willie
Wilson, Marine Biological Association of the UK; Erik Zettler, NIOZ Royal Netherlands
Institute for Sea Research and Utrecht University; Xiao-Hua Zhang, Ocean University of
China.
Chapter 1
Microbes in the
Marine Environment
Viewed from space, it is clear why our planet would be better named “Ocean” than “Earth.”
More than 70% of the planet’s surface is covered by interconnected bodies of water. Life
originated in the oceans about 3.5 billion years ago and microbes were the only form of life
for two-thirds of the planet’s existence. The development and maintenance of all other forms
of life depend absolutely on the past and present activities of marine microbes. Yet the vast
majority of humans—including many marine scientists—live their lives completely unaware
of the diversity and importance of marine microbes. Such understanding is vital, as we now
live in a period of rapid global change. This chapter introduces the scope of marine microbi-
ology, the different types of marine microbe (viruses, bacteria, archaea, fungi, and protists),
and their place in the living world. The activities of microbes in the many diverse habitats
found in the marine environment are introduced to provide the background for more detailed
consideration in later chapters.
Key Concepts
• Modern methods have led to new ideas about the diversity and evolution of microbial
life.
• Marine microbes are highly diverse and exist in huge numbers, forming a major com-
ponent of biomass on Earth.
• The most abundant marine microbes are exceptionally small.
• The oceans provide diverse specialized habitats, in which physical and chemical con-
ditions determine microbial activities.
• Planktonic microbes are responsible for primary productivity and recycling of organic
compounds in a continuum of dissolved and particulate matter.
• Microbes are important in the formation and fate of sediments and there is abundant
life below the seafloor.
• Microbes colonize the surfaces of inanimate objects and other living organisms by the
formation of biofilms and microbial mats.
2 Chapter 1
ORIGINS AND SCOPE OF MARINE MICROBIOLOGY

Marine microbiology has developed into one of
the most important areas of modern science
Ever since a detailed study of the microbial world began in the late nineteenth century, scien
tists have asked questions about the diversity of microbial life in the sea, its role in ocean pro
cesses, its interactions with other marine life, and its importance to humans. However, despite
excellent work by pioneering scientists, progress in understanding accumulated gradually and
some aspects were poorly understood until recently. However, toward the end of the twentieth
century, several factors conspired to propel marine microbiology to the forefront of “main
stream” science. The involvement of more investigators and the subsequent application of new
technology mean that it is now one of the most exciting and fast-moving areas of investigation.
Today, our subject is characterized by multidisciplinary investigations and widespread appli
cation of powerful new tools in molecular biology, information technology, remote sensing,
and deep-sea exploration, leading to astonishing discoveries of the abundance, diversity, and
interactions of marine microbial life and its role in global ecology. These continuing new dis
coveries necessitate radical rethinking of our understanding of ocean processes. We now real
ize the vital role that marine microbes play in the maintenance of our planet, a fact that will
have great bearing on our ability to respond to problems such as the increase in human popula
tion, overexploitation of fisheries, climate change, ocean acidification, and marine pollution.
Studies of the interactions of marine microbes with other organisms are providing intrigu
ing insights into the phenomena of food webs, symbiosis, pathogenicity, and the important
role microbiomes play in metazoan biology. Since some marine microbes produce disease or
damage, we need to study these processes and develop ways to control them. Finally, marine
microbes have beneficial properties such as the manufacture of new drugs and materials, and
the development of new processes in the growing field of marine biotechnology. This chapter
sets the scene for the discussion of all these topics in this book.
Microbes include microscopic cellular

organisms and non-cellular viruses
Defining the terms “microbiology” and “microorganism” is surprisingly difficult!
Microbiology is the study of very small organisms that are too small to be seen clearly with
the naked eye (i.e. less than about 1 mm diameter), but most microbiologists are concerned
with the activities or molecular properties of microbial communities rather than viewing indi
vidual cells with a microscope. The term “microorganism” simply refers to a form of life that
falls within the microscopic size range, but there is a huge spectrum of diversity concealed by
i TINY MICROBES…
HUGE NUMBERS
this all-encompassing term. Indeed, some “microorganisms” are large enough to see without
using a microscope, so this is not entirely satisfactory either. Some scientists would argue that
Whitman et al. (1998) estimated the distinguishing features of microorganisms are small size, unicellular organization, and
the total number of bacterial osmotrophy (feeding by absorption of nutrients). The osmotrophic characteristic is important
and archaeal cells in the oceans because diffusion processes are a major limitation to cell size, as discussed in the next sec
to be about 1029. This figure was
tion. However, this characteristic would exclude many microscopic unicellular eukaryotes,
confirmed by Bar-On et al. (2018)
in a recent recalculation based on
many of which feed by phagotrophy (engulfment of particles). For many years, these micro
analysis of many new datasets; organisms were studied by specialists who had a traditional background in botany or zoology
they also estimated the biomass and classified into “plant-like” (algae) or “animal-like” (protozoa) groups. However, many of
of marine bacteria and archaea these organisms are mixotrophic and can switch from photosynthesis to phagotrophic feed
at 1.3 and 0.3 gigatons (Gt) of ing, so the “plant” or “animal” similarity is meaningless. This loose grouping of organisms
carbon, respectively. Suttle (2005) is therefore called “protists,” a diverse category encompassing most of the diversity within
calculated the number of viruses the domain Eukarya. Depending on their size (see below), they may also be referred to as
to be about 1030 —again, this was microeukaryotes or picoeukaryotes. The study of marine protists and recognition that they
confirmed by Bar-On et al. (2018). are microbes with a major role in ocean processes has lagged behind the study of bacteria
This is an unimaginably huge num
until recently. Where do viruses fit? Viruses are obviously microscopic, so I consider them to
ber—1 million, million, million, mil
be microbes. However, they are not cellular, so cannot be described as microorganisms and
lion, million. If all the marine virus
particles were placed end to end, many would argue that they are not living (this question is explored in depth in Chapter 7).
they would span about 10 million In summary, in this book I use the term “microbe” as a generic descriptor for microscopic
light years (100 times the distance cellular organisms including bacteria, archaea, fungi, and protists, together with the non
across our own galaxy). cellular viruses.
Microbes in the Marine Environment 3
Marine microorganisms are found in all

three domains of cellular life
Biologists usually rely on the study of morphology and physiological properties to classify living
organisms, but these characteristics have always proved frustratingly unhelpful when dealing
with microbes. Modern methods of classification group organisms by attempting to determine
the evolutionary relationships. Such phylogenetic systems of classification depend on compari
sons of the genetic information contained in their macromolecules, especially nucleic acids and
proteins. If two organisms are very closely related, we expect the sequence of the individual units
(nucleotides or amino acids) in a macromolecule to be more similar than they would be in two
unrelated organisms. In the 1970s, Carl Woese and colleagues pioneered the use of ribosomal
RNA (rRNA) sequencing in order to develop a better view of microbial diversity. Our view of the
living world has since been revolutionized by advances in this approach, made possible because
of the parallel advances in molecular biological techniques and computer processing of the large
amounts of information generated. Because the secondary structure of rRNA is so important in
the ribosome and the vital cell function of protein synthesis, base sequence changes in the rRNA
molecule occur quite slowly in evolution. In fact, some parts of rRNA are highly conserved and
sequence comparisons can be used to ascertain the similarity of organisms on a broad basis. The
methods and applications of this major technique are described in Chapter 2.
In 1990, Woese identified three distinct lineages of cellular life, referred to as the domains
Archaea, Bacteria, and Eukarya. A phylogenetic “tree of life” based on rRNA sequences
envisaged divergence of these three domains from an original “universal ancestor”
(Figure 1.1A). A phylogenetic approach to classification is now widely accepted, although
some biologists prefer other systems. Microbiologists like it because we can say that we study
two entire domains of life and a significant proportion of the third! Traditionally, members of
the domains Bacteria and Archaea have been grouped together as “the prokaryotes,” because
they share a simple internal cellular structure without a nucleus. However, the most impor
tant consequence of the three-domain tree of life is that we now realize that the Bacteria and
Archaea are completely different phylogenetic groups. Archaea are not a peculiar, specialized
Figure 1.1 Representations of the

three domains of life. A. Simple
tree based on early interpretation
of ribosomal RNA sequencing. In
this model, the root of the tree is
envisaged as a hypothetical universal
ancestor from which all life evolved.
B. A three-domain tree based on
evidence of extensive lateral gene
transfer, revealed by studies of other
genes. (Drawn before discovery of
other archaeal branches; see Box 5.1).
C. An artistic representation of major
divisions of the tree of life by Hug
et al. (2016). The numerous known
groups of the Bacteria are shown on
the left, with the large group of cur-
rently uncultivable Bacteria termed
the Candidate Phyla Radiation at
upper right. The Archaea are shown
at the left of the lower branch, with
the Eukarya at the lower right. (See
Figure 4.1 for an updated detailed
version of the tree). Credits: B. Gary
J. Olsen, University of Illinois, based
on concept of W. Ford Doolittle. C.
Zosia Rostomian, Berkeley Lab.
4 Chapter 1
group of bacteria as originally thought (for many years they were called the archaebacteria)
?
TWO DOMAINS but are in fact a completely separate group that actually has closer phylogenetic relation
OR THREE? ships to the Eukarya than to the Bacteria. This concept has proved to be very influential
There are many differences of in shaping our thinking about the evolution of organisms. As new methods and knowledge
opinion about the relationships about genomes has developed, the simple three-domain tree has changed, as illustrated in
between organisms, especially Figures 1.1B and 1.1C. These developments are discussed in detail in Chapters 4 and 5.
when we try to explain deep
evolutionary branches. Some The members of the Eukarya domain are the protists, fungi, plants, and animals. Their cells
authors believe that new evidence are distinguished by a membrane-bound nucleus and organelles with specific functions.
about the evolution of rRNA and
Mitochondria occur in all eukaryotic cells, with the exception of a few anaerobic protozoa, and
the use of new models to compute
phylogenetic trees calls the three-
carry out the processes of respiratory electron transport. In photosynthetic eukaryotes, chlo
domain tree concept into ques roplasts carry out reactions for the transfer of light energy for cellular metabolism. Various
tion. Embley and Williams (2016) lines of evidence (especially the molecular analysis of the nucleic acids and proteins) support
argue that the discovery of new the “endosymbiosis theory” (originally developed by Lynn Margulis in the 1960s) that the
archaeal groups (see Chapter 5) organelles of eukaryotic cells have evolved by a process of endosymbiosis, in which one cell
supports the idea of a two-domain lives inside another cell for mutual benefit. This theory proposes that the original source of
“eocyte” tree to explain the origin mitochondria in eukaryotic cells occurred when primitive cells acquired respiratory bacteria
of the eukaryotes from within the (most closely related to proteobacteria) and that the chloroplasts evolved from endosymbiosis
Archaea. The “archaeal ances with cyanobacteria. Such interactions between different types of cell have continued through
tor hypothesis” for the origin of
out evolution, and Chapter 10 contains many examples of endosymbiosis involving microbes.
eukaryotes is gaining acceptance,
although Forterre (2015) and Nasir
et al. (2016) provide alternative
explanations. Horizontal gene transfer confounds
our understanding of evolution
The use of rRNA sequences as a basis for phylogenetic classification has revolutionized
our understanding of microbial diversity and phylogeny. However, since advances in DNA
sequencing (see Chapter 2) made it possible to study the sequences of many other genes,
we have found increasing evidence of extensive horizontal gene transfer (HGT, also known
as lateral gene transfer, LGT) between microbes. Such transfers occur most commonly
between related organisms but transfers across bigger genetic distances also occur—even
between domains. Members of the Bacteria and Archaea contain some genes with very simi
lar sequences, and members of the Eukarya contain genes from both of the other domains.
Some members of the domain Bacteria have even been shown to contain eukaryotic genes.
Previously, evolution was explained only by the processes of mutation and sexual recombina
tion, but we now know that the pace of evolution is accelerated by the transfer and acquisition
of modules of genetic information. This phenomenon is widespread in modern members
of the Bacteria and Archaea and can occur via three processes. During the process known
as transformation, cells may take up and express naked DNA from the environment, while
conjugation relies on cell–cell contact mediated by pili. The most important source of HGT
is the process of transduction by phages (viruses infecting bacterial or archaeal cells and
introducing “foreign” DNA); this is explored in detail in Chapter 7. The enormous diversity
of marine viruses and the identification of a viral origin of genes in many marine organisms
indicate how important this process has been throughout evolution.
Viruses are non-cellular entities with great

importance in marine ecosystems
Virus particles (virions) consist of a protein capsid containing the viral genome composed of
either RNA or DNA. Because they only contain one type of nucleic acid, viruses must infect
living cells and take over the host’s cellular machinery in order to replicate. It is often thought
that viruses could have evolved (perhaps from bacteria) as obligate parasites that have progres
sively lost genetic information until they consist of only a few genes, or that they represent
fragments of host-cell RNA or DNA that have gained independence from cellular control. New
ideas about the evolution of viruses are discussed in Chapter 7. The genome of viruses often
contains sequences that are equivalent to specific sequences in the host cell. Viruses exist for
every major group of cellular organisms (Bacteria, Archaea, Fungi, protists, plants, and ani
mals), but at present we have knowledge of only a tiny proportion of the viruses infecting
marine life. As discussed in Chapter 7, recognition of the abundance and diversity of marine
viruses, and the role that they play in biogeochemical cycles and the control of diversity in
marine microbial communities, has been one of the most important discoveries of recent years.
? TIME TO CHOP DOWN
THE “TREE OF LIFE”?
The idea that relationships
Microbial processes shape the living world between all living organisms can
be represented as a tree of life
Probably the most important overriding features of microbes are their exceptional diversity
helped to shape Darwin’s theory
and ability to occupy every conceivable habitat for life. Indeed, what we consider “conceiv
of evolution by natural selection
able” is challenged constantly by the discovery of new microbial communities in habitats and has been deeply embed-
previously thought of as inhospitable or carrying out processes that we had no idea were ded in the philosophy of biology
microbial in nature. Bacteria and archaea have shaped the subsequent development of life for more than 150 years. As the
on Earth ever since their first appearance—the metabolic processes that they carry out in importance of endosymbiosis and
the transformation of elements, degradation of organic matter, and recycling of nutrients HGT became better understood,
play a central role in innumerable activities that affect the support and maintenance of all some evolutionary scientists began
other forms of life. Microbial life and the Earth have evolved together, and the activities of to question the validity of the
microbes have affected the physical and geochemical properties of the planet. Indeed, they “tree of life” concept. A seminal
are actually the driving forces responsible for major planetary processes like changes in the paper by Doolittle (1999) argued
that “Molecular phylogeneticists
composition of the atmosphere, oceans, soil, and rocks. This is especially relevant to our
will have failed to find the ‘true
consideration of the marine environment, in view of the huge proportion of the biosphere tree’, not because their methods
that this constitutes. Despite the preponderance of microbes and the importance of their are inadequate or because they
activities, they are unseen in everyday human experience. Microbes live and grow almost have chosen the wrong genes, but
everywhere, using a huge range of resources, whereas plants and animals occupy only a small because the history of life cannot
subset of possible environments and have a comparatively narrow range of lifestyles. properly be represented as a tree.”
Relationships are now envisaged
as complex intertwined branches,
Marine microbes show great variation in size more like a web (Figure 1.1B) or
network of genomes (Dagan and
Table 1.1 shows the range of dimensions and volumes of some representative marine microbes. Martin, 2009). However, this
Even by the usual standards of microbiology, the most abundant microbes found in seawater remains a controversial topic, and
are exceptionally small—much smaller than implied by the common textbook or internet some have argued that analysis
statement that “bacteria are typically a few micrometers in length.” Their very small size is of genome sequences for “core
the main reason that appreciation of their abundance eluded us for so long. As described in genes” still supports the idea of a
Chapter 2, recognition of the abundance of marine microbes depended on the development common ancestor and branching
of fine-pore filters and direct counting methods using epifluorescence microscopy and flow tree (Ciccarelli et al., 2006)—an
cytometry. Small cell size has great significance in terms of the physical processes that affect approach that worked successfully
for Hug et al. (2016) to develop a
life. At the microscale, the rate of molecular diffusion becomes the most important mecha
new tree of all major groups of life
nism for transport of substances into and out of the cell. Small cells feeding by absorption
(Figure 1.1C).
(osmotrophy) can take up nutrients more efficiently than larger cells. The surface area to
volume ratio (SA/V) is the critical factor because as cell size increases, volume (V) increases
more quickly than surface area (SA), as shown in Figure 1.2A.
The most abundant ocean bacteria and archaea have very small cell volumes and large SA/V
ratios. The majority are smaller than about 0.6 μm in their largest dimension, and many are
less than 0.3 μm, with cell volumes as low as 0.003 μm3. Indeed, the most abundant type
of organism in the oceans (the SAR11 clade, Figure 1.3A) has some of the smallest known
cells. If nutrients are severely limiting, as they are in most of the oceans, selection will favor
small cells. Since the first description of such small cells, termed “ultramicrobacteria,” their
size has provoked considerable controversy. Such extremely small cells could result from a
genetically fixed phenotype maintained throughout the cell cycle or because of physiologi
cal changes associated with starvation. The latter explanation is supported by the fact that
some cultured bacteria become much smaller when starved. Most naturally occurring bacteria
(identified only by their genetic “signature”) have been impossible to grow in culture—this
is a central problem in marine microbiology, which we shall return to on several occasions
in future chapters. Because of this, it has been difficult to determine whether small size is a
genotypically determined condition for marine bacteria. However, studies with some recently
cultured marine bacteria from low-nutrient (oligotrophic) ocean environments show that addi
tion of nutrients does not cause an increase in cell size. Cells use various strategies to increase
the SA/V ratio and thus improve efficiency of diffusion and transport. In fact, spherical cells
are the least efficient shape for nutrient uptake, and many marine bacteria and archaea are
thin rods or filaments or may have appendages such as stalks or buds. Figure 1.2B shows
examples of the diverse morphology of marine bacteria in a sample of ocean water. Many of
6 Chapter 1
Table 1.1 Size range of some representative marine microbes
Organism Characteristics Size Volume

(μm)a (μm3)b
Brevidensovirus Icosahedral DNA virus infecting shrimp 0.02 0.000004
Coccolithovirus Icosahedral DNA virus infecting Emiliania huxleyi 0.17 0.003
Thermodiscus Disc-shaped. Hyperthermophilic archaeon 0.2 × 0.08 0.003
“Ca. Pelagibacter ubique”c Crescent-shaped bacterium ubiquitous in ocean plankton (cultured 0.1 × 0.9 0.01
example of SAR11 clade)
Megavirus chilensis Giant virus infecting marine amoebae 0.44 0.045
Prochlorococcus Cocci. Dominant photosynthetic ocean bacterium 0.6 0.1
Ostreococcus Cocci. Prasinophyte alga. Smallest known eukaryote 0.8 0.3
Vibrio Curved rods. Bacteria common in coastal environments and associated 1×2 2
with animals and human diseases
Pelagomonas calceolata Photosynthetic flagellate adapted to low light 2 24
Pseudo-nitzschia Pennate diatom which produces toxic domoic acid 5 × 80 1600
Staphylothermus marinus Cocci. Hyperthermophilic archaeon 15 1800
Thioploca auraucae Filamentous. Sulfur bacterium 30 × 43 30000
Lingulodinium polyedra Bioluminescent bloom-forming dinoflagellate 50 65000
Beggiatoa Filamentous. Sulfur bacterium 50 × 160 314000
Epulopiscium fishelsoni Rods. Bacteria symbiotic in fish gut 80 × 600 3000000
Thiomargarita namibiensis Cocci. Sulfur bacterium 300d 14137100

aApproximate diameter × length; where one value is given, this is the diameter of spherical virus particles or cells. bApproximate values calculated
assuming spherical or cylindrical shapes. cCandidatus, provisional taxonomic name—see Chapter 4. dCells up to 750 μm have been recorded.
the larger organisms overcome the problems of diffusion by having extensive invaginations of
the cytoplasmic membrane or large intracellular vacuoles, increasing the SA. Small cell size
also has important implications for mechanisms of active motility and chemotaxis, because of
the microscale effects of Brownian movement (bombardment by water molecules) and shear
forces. Small marine bacteria have mechanisms of motility and chemotaxis quite unlike those
with which we are familiar from laboratory studies of organisms such as Escherichia coli.
As shown in Table 1.1, marine eukaryotic microbes also show a considerable variation in
size. Many protists have cellular dimensions that are more typical of the familiar bacteria.
The smallest known eukaryote is Ostreococcus tauri, which is only about 0.8 μm in diameter
(Figure 1.3B). Again, the realization that such small cells (now referred to as “picoeukary-
otes”) play a key role in ocean processes escaped attention until quite recently. Many small
protists seem capable of engulfing bacteria of almost the same size as themselves or can prey
on much larger organisms. Many groups of the flagellates, ciliates, diatoms, and dinoflagel-
lates are somewhat larger, reaching sizes up to 200 μm, and amoeboid types (radiolarians and
foraminifera) can be millimeters in diameter. Finally, a few types of bacteria can be bigger
than many protists. The largest of these is Thiomargarita namibiensis (Figure 1.3C). Further
discussion of the size range of microbes is given in the section on plankton below.
OCEAN HABITATS
The world’s oceans and seas form an
interconnected water system
The oceans cover 3.6 × 108 km2 (71% of the Earth’s surface) and contain 1.4 × 1021 liters of
water (97% of the total on Earth). The average depth of the oceans is 3.8 km, with a number
of deep-sea trenches, the deepest of which is the Marianas Trench in the Pacific (11 km). The
Figure 1.2 (a) Diagrammatic rep-

resentation of three spherical cells
showing a reduction in the ratio
of surface area (SA) to volume (V)
as size increases. V is a function of
r = 1.0 µm r = 2.0 µm r = 3.0 µm the cube of the radius (V = (4 / 3)πr 3 )
SA = 12.6 µm2 SA = 50.3 µm2 SA = 113.1 µm
2
V = 4.2 µm3 V = 33.5 µm3 V = 113.1 µm

3 whereas SA is a function of the
square of the radius (SA = 4πr2). Cells
with large SA/V ratios are more
efficient at obtaining scarce nutrients
by absorption across the membrane.
(b) Scanning electron micrograph
of picoplankton, showing various
cell morphologies of marine bac-
SA/V = 3.0 SA/V = 1.5 SA/V = 1.0 teria (cells are artificially colorized
(a) for effect). Bar represents ~ 1 μm.
Credit: Ed DeLong, Massachusetts
Institute of Technology.
(b)
ocean floor contains large mountain ranges and is the site of almost all the volcanic activity
on Earth. More than 80% of the area and 90% of the volume of the oceans occurs beyond the
continental shelf. Most of the deep-sea remains unexplored. It is usual to recognize five major
ocean basins, although they actually form one interconnected water system.
The Pacific is the deepest and largest ocean, almost as large as all the others combined. This
single body of water has an area of 1.6 × 108 km2. The ocean floor in the eastern Pacific is
dominated by the East Pacific Rise, while the western Pacific is dissected by deep trenches.
The Atlantic Ocean is the second largest with an area of 7.7 × 107 km2 lying between Africa,
Europe, the Southern Ocean, and the Americas. The mid-Atlantic Ridge is an underwater
mountain range stretching down the entire Atlantic basin and the deepest point is the Puerto
Rico Trench (8.1 km). The Indian Ocean has an area of 6.9 × 107 km2 and lies between Africa,
the Southern Ocean, Asia, and Australia. A series of ocean ridges cross the basin, and the
deepest point is the Java Trench (7.3 km). The Southern Ocean is the body of water between
60°S and Antarctica. It covers 2.0 × 107 km2 and has a fairly uniform depth of 4–5 km, with
a continual eastward water movement called the Atlantic Circumpolar Current. The Arctic
Ocean, lying north of the Arctic Circle, is the smallest ocean, with an area of 1.4 × 107 km2. As
well as the major oceans, there are marginal seas, including the Mediterranean, Caribbean,
Baltic, Bering, South China Seas, and many others.
At the margins of major landmasses, the ocean is shallow and lies over an extension of the
land called the continental shelf. This extends offshore for a distance ranging from a few
kilometers to several hundred kilometers and slopes gently to a depth of about 100–200 m,
8 Chapter 1
Figure 1.3 Extremes of size in

marine microbes (note different scale
bars). A. Cryo-electron tomography
of “Candidatus Pelagibacter ubique”
cells, one of the smallest bacteria
known (a cultivated representative
of the abundant SAR11 clade). Left:
a tomographic slice of a typical log-
phase cell. Right: the 3D isosurface-
rendered model of the same cell
reveals internal cellular organization.
Model coloring: outer membrane
(blue), inner membrane (cyan),
peptidoglycan (white), cytoplasm
(orange), nucleoid (red), ribosome-
like particles are represented by
yellow spheres. B. Transmission
electron micrograph (TEM) of sec-
tion of Ostreococcus tauri, the small-
est known eukaryote. N = nucleus,
m = mitochondrion, c = chloroplast.
C. Light micrograph of Thiomargarita
namibiensis, the largest known
bacterium, showing sulfur gran-
ules. Credits: A. Xiaowei Zhao and
Daniela Nicastro, University of
Texas SW Medical Center, Stephen before there is a steeper drop-off to become the continental slope. The abyssal plain covers
Giovannoni, Oregon State University, much of the ocean floor; this is a mostly flat surface with few features, but is broken in vari
and J. Richard McIntosh, University ous places by ocean ridges, deep-sea trenches, undersea mountains, and volcanic sites.
of Colorado. B. Reprinted from
Henderson et al. (2007), CC-BY-2.0.
C. Heide Schulz-Vogt, Max Planck The upper surface of the ocean is in
Institute for Marine Microbiology, constant motion owing to winds
Bremen.
Rotation of the Earth deflects moving air and water in a phenomenon known as the Coriolis
Effect. Wind belts created by differential heating of air masses move the surface water, and in
combination with the Coriolis Effect they generate major surface current systems. This leads
to large circular gyres that move clockwise in the northern hemisphere and anticlockwise
in the southern hemisphere. Such gyres and currents affect the distribution of nutrients and
marine organisms. On the basis of surface ocean temperatures, the marine ecosystem can be
divided into four major biogeographical zones, namely polar, cold temperate, warm temper
ate (subtropical), and tropical (equatorial). The boundaries between these zones are roughly
defined by latitude but are strongly affected by surface currents moving heat away from the
equator, as well as varying with the season.
Deep-water circulation systems transport

water between the ocean basins
Below a depth of about 200 m, ocean water is less affected by mixing and wind-generated
currents. However, a system of vast undersea rivers transports water around the globe and
has a major influence on the distribution of nutrients (Figures 1.4 and 8.1). This ther
mohaline circulation system—often referred to as the “global ocean conveyor belt”—is
formed by the effects of temperature and salinity causing differences in the density of
water. Surface water in the North Atlantic flows toward the pole as the Gulf Stream. Water
is removed to the atmosphere by evaporation and during the formation of sea ice in high
latitudes, resulting in higher salinity. The cold, salty water becomes denser and sinks to
form a deep pool, which then flows south toward Antarctica, where more cold, dense water
is added. The current then splits, with one branch going toward the Indian Ocean and the
other to the Pacific Ocean. As the current nears the equator it warms and becomes less
dense, so upwelling occurs. The warmer waters loop back to the Atlantic Ocean, where
they start the cycle again.
Figure 1.4 A. The thermohaline

circulation system (global ocean
“conveyor belt”). (Credit: NASA/JPL.)
B. Approximate locations of the
major warm (red) and cold (blue)
ocean currents and the gyres in the
South Pacific (SPG), North Pacific
(NPG), North Atlantic (NAG), South
Atlantic (SAG), and Indian Ocean
(IOG).
Light and temperature have important

effects on microbial processes
Light is of fundamental importance in the ecology of microbes that use light energy for photo
synthesis and other functions, thus affecting primary productivity. The extent to which light of
different wavelengths penetrates seawater depends on a number of factors, notably cloud cover,
the polar ice caps, dust in the atmosphere, and variation of the incident angle of solar radiation
according to season and location on the Earth’s surface. Light is absorbed or scattered by organ
isms and suspended particles. Even in the clearest ocean water, photosynthesis is restricted by
the availability of light of sufficient intensity to the upper 150–200 m (Figure 1.5). This is termed
the photic or euphotic zone (from the Greek for “well lit”). Blue light has the deepest penetration,
and photosynthetic microbes at the lower part of the photic zone have light-harvesting systems
that are tuned to collect blue light most efficiently (p.134). In turbid coastal waters, during sea
sonal plankton blooms, the euphotic zone may be only a few meters deep, and green and yellow
light have the deepest penetration. Solar radiation also heats surface waters and leads to thermal
stratification of seawater. In tropical seas, the continual input of energy from sunlight leads to
warming of the surface waters to 25–30°C, causing a considerable difference in density from
that of deeper waters. Thus, throughout the year, there is a marked thermocline at about 100–150
m, below which there is a sudden reduction in temperature to 10°C or less. Little mixing occurs
between these layers. In polar seas, the water is permanently cold except for a brief period in
the summer, when a slight thermocline develops. Apart from this period, turbulence created by
surface winds generates mixing of the water to considerable depths. Temperate seas show the
greatest seasonal variation in the thermocline, with strong winds and low temperatures leading
to extensive mixing in the winter. The thermocline develops in the spring, leading to a marked
shallow surface layer of warmer water in summer. As the sea cools and wind increases, the ther
mocline breaks down again in the autumn. Combined with seasonal variations in light intensity,
these effects of temperature stratification and vertical mixing have a great impact on rates of
photosynthesis and other microbial activities that affect the entire trophic system.
10 Chapter 1
Figure 1.5 Penetration of light of

different wavelengths in seawater.
Credit: Kyle Carothers, NOAA-OE.
Microbes occur in all the varied

habitats found in the oceans
Various ecological zones can be recognized in the marine environment, as shown in
Figure 1.6. Microbes are found everywhere—as members of the plankton, associated with
suspended particles and colloidal materials, attached to surfaces like rocks and submerged
structures, in association with plants and animals, or in sediments.
Plankton is a general term in marine biology referring to organisms suspended in the water
column that do not have sufficient power of locomotion to resist large-scale water currents (in
contrast to the nekton, which are strong-swimming animals). Traditionally, biologists refer
to phytoplankton (plants) and zooplankton (animals). Using this approach, we can add the
terms bacterioplankton for bacteria, virioplankton for viruses, and mycoplankton for fungi.
Traditional concepts of “plant” and “animal” are now unsatisfactory, and the term phytoplank
? WHY IS THE
SEA SALTY?
ton therefore refers to all photosynthetic microbes, including cyanobacteria, as well as algae
and other eukaryotic protists. Of course, phytoplankton is only active in the photic zone, but
The constant percolation of rain- heterotrophic protists are found at all depths, where active bacterial and archaeal production
water through soil and rocks leads provides their food source. Another approach to classifying the plankton is in terms of size
to weathering, in which some of classes, for which a logarithmic scale ranging from megaplankton (>20 mm) to femtoplankton
the minerals are dissolved. Ground (<0.2 μm) has been devised. Table 1.2 shows the size classes that encompass marine microbes.
water has very low levels of salts Thus, the viruses constitute the femtoplankton, and bacteria and archaea mainly occur in the
and we cannot taste it in the water picoplankton. The recently discovered giant viruses (see Chapter 7) may also be considered
we drink. The addition of salts to to be part of the picoplankton size range. While protists (eukaryotic microbes) have a wide
the oceans from rivers is thus a size range and occur in the picoplankton, nanoplankton, and microplankton, we now know
very slow process, but evaporation
that in most marine samples, the majority of protistan cells are in the picoplankton range. This
of water from the oceans to form
clouds means that the salt concen- system of tenfold progression is not rigorously adhered to, and many investigators define pico
tration has increased to its present plankton as organisms ≤3 µm. (This cut-off value provides a more coherent pattern in surveys
level over hundreds of millions of to estimate seasonal or geographic changes in abundance of small eukaryotes measured by
years. Seawater also percolates into filtration). Because individual taxa of photosynthetic and heterotrophic protists can span these
the ocean crust where it becomes three size ranges, this system is of little use in identification and classification. However, it is
heated and dissolves minerals, useful for specifying the size ranges that are likely to be collected using filters or meshes with
emerging at hydrothermal vents different cut-off values. It is also useful when considering the feeding of heterotrophic protists,
(Figure 1.13). Submarine volcanoes which generally graze by phagocytosis of organisms in the next size class down. Although
also result in reactions between there are important exceptions, the predator–prey size ratio is typically about 10:1.
seawater and hot rock, resulting in
the release of salts. The salt con-
centration in the oceans appears to Seawater is a complex mixture of inorganic and
be stable, with deposition of salts
in sediments balancing the inputs organic compounds, colloids, and gels
from weathering, hydrothermal
Seawater is a slightly alkaline (pH 7.5–8.4) aqueous solution—a complex mixture of more
vents, and volcanic activity.
than 80 solid elements, gases, and dissolved organic substances. The concentration of these
Estuarine and intertidal Figure 1.6 The major ecological

Epibionts: inanimate objects, detritus zones of the oceans and marine
Estuarine and intertidal Photic zone Plankton and marine snow microbial habitats (not to scale).
Epi- and endobionts: Epi- and endobionts: Epi- and endosymbionts,
coastal plants and animals algae and animals pelagic animals
Depth (m)
Neuston
0
Littoral Cold seeps Epipelagic
(coastal) 100–200
Shelf Mesopelagic
10°C 700–1000
Slope Bathypelagic
<4°C 2000–4000
Hydrothermal vents Abyssopelagic
Sediments, reefs, vents
and seeps. Epi- and Abyssal
endobionts: benthic animals 6000
plain
Hadalpelagic
Neritic (shelf) Deep-sea

10 000
trench
varies considerably according to geographic and physical factors, and it is customary to refer
to the salinity of seawater in parts per thousand (‰) to indicate the concentration of dissolved
substances. The open ocean has a salinity in the range 34–37‰, with differences in different
regions due to dilution by rainfall and evaporation. Oceans in subtropical latitudes have the
highest salinity as a result of higher temperatures, while temperate oceans have lower salinity
as a result of less evaporation. In coastal regions, seawater is diluted considerably by fresh-
water from rivers and terrestrial runoff and is in the range 10–32‰. Conversely, in enclosed
areas such as the Red Sea and Arabian Gulf, the salinity may be as high as 44‰. In polar
areas, the removal of freshwater by the formation of ice also leads to increased salinity. The
major ionic components of seawater are sodium (55% w/v), chloride (31%), sulfate (8%), mag-
nesium (4%), calcium (1%), and potassium (1%). Together, these constitute more than 99%
of the weight of salts. There are four minor ions—namely bicarbonate, bromide, borate, and
strontium—which together make up just less than 1% of seawater. Many other elements are
present in trace amounts (<0.01%), including key nutrients such as nitrate, phosphate, silicate,
and iron. The concentration of these is crucial in determining the growth of marine microbes
and the net productivity of marine systems, as discussed in Chapter 9.
Table 1.2 Classification of plankton by size
Size category Size Examples of microbial groups

range
(μm)
Femtoplankton 0.01–0.2 Virusesa
Picoplankton 0.2–2 (3)b Bacteriac, archaea,

prasinophytes, haptophytes,
some flagellates
Nanoplankton 2–20 Coccolithophores, diatoms,

dinoflagellates, flagellates
Microplankton 20–200 Ciliates, diatoms,

dinoflagellates, foraminifera,
yeasts
aSome giant viruses are >1 µm long. bA value of ≤3 µm is most commonly used, see text. cSome
filamentous cyanobacteria and sulfur-oxidizing bacteria occur in larger size classes (see Table 1.1).
12 Chapter 1
The concentration of salts has a marked effect on the physical properties of seawater. The
freezing point of seawater at 35‰ is −1.9°C, and seawater increases in density up to this point.
As noted above, this results in the formation of masses of cold, dense water in polar regions,
which sink to the bottom of the ocean basins and are dispersed by deep-water circulation cur
rents. Differences in the density of seawater create a discontinuity called the pycnocline, which
separates the top few hundred meters of the water column from deeper water. This has great
significance, because the gases oxygen and carbon dioxide are more soluble in cold water.
Oxygen is at its highest concentrations in the top 10–20 m of water, owing to exchange
with the atmosphere and production of oxygen by photosynthetic plankton. Concentration
decreases with distance from the surface until it reaches a minimum between 200 and 1000
m, and bacterial decomposition of organic matter may create conditions that are almost
anoxic. Below this, the oxygen content increases again as a result of the presence of dense
water (with increased solubility at lower temperature) that has sunk from polar regions and
been transported on the thermohaline circulation system. This oxygen gradient varies greatly
in different regions, and there are several regions where large bodies of hypoxic water occur
at relatively shallow depths—these are the oxygen minimum zones (Figure 9.7).
The solubility of carbon dioxide is an important factor in controlling the exchange of carbon
between the atmosphere and the oceans and therefore is of huge significance in understand
ing climatic processes, as discussed in Chapter 8. Only a very small proportion of dissolved
inorganic carbon (DIC) is present in the form of dissolved CO2 gas. Carbon dioxide reacts
with water to form carbonic acid, which rapidly dissociates to form bicarbonate, hydrogen
ions, and carbonate in the reactions:
CO2 (gas) + H 2O � H 2 CO3 � H + + HCO3 − � 2H + + CO32−
These reactions tend to stay in equilibrium, buffering the pH of seawater within a narrow
range and constraining the amount of CO2 taken up from the atmosphere. However, the
IS “DISSOLVED
? ORGANIC MATTER”
REALLY DISSOLVED?
increasing atmospheric levels of CO2 since the industrial revolution are shifting the equilib
rium and causing the pH to fall because of increased levels of H+ ions, leading to the phe
nomenon known as ocean acidification, which may have major consequences for ocean life.
Oceanographers tradition-
ally describe organic matter as It is tempting to think of seawater as a homogeneous fluid, with planktonic microbes and nutri
“dissolved” and “particulate’ ents evenly distributed within it. However, a growing body of evidence indicates that there
(DOM and POM, respectively).
is microscale heterogeneity in the distribution of nutrients around organisms and particles of
Measurements of concentrations
organic matter. Large-scale processes like productivity, nutrient recycling, and geochemical
and fluxes of DOM and its con-
stituent elements carbon (DOC), cycles are the result of microbial activity. In turn, physical processes like turbulence, pho
nitrogen (DON), and phospho- ton flux, and gas exchange are translated down to the microscale level, affecting microbial
rus (DOP) are among the most behavior and metabolism. Physical factors such as diffusion, shear forces, and viscosity must
important factors in the study of be considered in this context. A pool of small, soluble organic molecules provides the starting
ocean processes. It is important material for bacterial productivity and recycling or carbon compounds that drives ocean food
to remember that the difference webs (see Chapter 8). Only molecules of less than about 600 Da can be assimilated across the
between “dissolved” and “particu- membrane—any larger molecules must be broken down by extracellular enzymes. Seawater
late” is a purely empirical distinc- contains vast amounts of polymers in the form of proteins, carbohydrates, and nucleic acids,
tion, reflecting the size of filters resulting from excretion by organisms or the release of their cellular material by lysis. Free
used in sample preparation. There
dissolved organic matter (DOM) in the form of polymeric macromolecules can spontane
is no absolute definition, but most
filters used in studies of DOM and
ously assemble to form gels in surface waters, which coalesce to form larger aggregates
POM have pore sizes from about that diffuse into the bulk seawater. It is estimated that at least 10% of organic carbon in the
0.45 to 1.0 μm. Many bacteria oceans exists in this form. We can envisage seawater as a complex three-dimensional gel-like
and almost all viruses would pass network with a continuum between dissolved, colloidal, and particulate material (Figure 1.7).
through such filters and there- As a result, at a micrometer scale—the realm of the microbes—there is great patchiness in
fore appear in the DOM fraction! the distribution of nutrients and the physical properties of microenvironments.
Colloidal material and polymers
aggregate to form particles, and it These microgels can further coalesce into larger structures termed transparent exopolymeric
is only low-molecular-weight com- particles (TEP). These are especially important in the carbon cycle, because they are criti
pounds like sugars and amino acids
cal in promoting the formation of particles that are sufficiently dense to sink through the
that are truly dissolved. Thus, DOM
water column, depositing carbon in the depths of the ocean and its sediments. This con
and POM form a continuum, with
microbes spanning both fractions. tinuous shower of clumps and strings of material which falls through the water column is
termed “marine snow” because of its resemblance to falling snowflakes when illuminated
Figure 1.7 Representation of the

size continuum of marine particles,
indicating the size range of plank-
tonic microbes and methods used
to study the different fractions.
Reprinted from Verdugo et al. (2004)
with permission from Elsevier.
underwater. Marine snow consists of aggregates of plankton cells, detritus from dead or
dying plankton, zooplankton fecal material, and inorganic particles, glued together by the
matrix of TEP released from plankton (Figure 1.8). Most particles are 0.5 to a few microme
ters in diameter, but they can grow to several centimeters in calm waters. Dissolved polymers
aggregate to form nanogels, stabilized by calcium binding. Larger aggregates form microgels
as a result of collision and coagulation of primary particles, and they increase in size as they
acquire more material through these physical processes. The nucleus for snow formation is
often the mucus-based feeding structures used by salps and larvaceans in the zooplankton.
Dying diatoms, at the end of a bloom, often precipitate large-scale snow formation owing to
the production of large amounts of mucopolysaccharides in their cell walls. The generation
of water currents during feeding by flagellates and ciliates colonizing the aggregate also col
lects particles from the surrounding water and leads to growth of the snow particle.
Marine snow is mainly produced in the upper 100–200 m of the water column, and large par
ticles can sink up to 100 m per day, allowing them to travel from the surface to the ocean deep
within a matter of days. This is the main mechanism by which a proportion of the photosyn
thetically fixed carbon is transported from the surface layers of the ocean to deeper waters
and the seafloor. However, aggregates also contain active complex assemblages of bacteria and
protists that graze on them. Levels of microorganisms in marine snow are typically 108–109
mL−1, which are about 100–10000-fold higher than in the bulk water column. As particles sink,
organic material is degraded by extracellular enzymes produced by the resident microbial pop
ulation. Microbial respiration creates anoxic conditions, so that diverse aerobic and anaerobic
microbes colonize different niches within the snow particle. The rate of solubilization exceeds
the rate of remineralization, so dissolved material leaks from snow particles, leaving a plume of
nutrients in its wake as it spreads by diffusion and advection. This may send chemical signals
that attract small zooplankton to consume the particle as food. The trailing plume also provides
a concentrated nutrient source for suspended planktonic bacteria, which may show chemotac
tic behavior in order to remain within favorable concentrations. Thus, much of the carbon is
recycled during its descent, but some material reaches the ocean bottom, where it is consumed
by benthic organisms or leads to the formation of sediments. Photosynthesis by algae and bac
teria leads to the formation of organic material through CO2 fixation, but viruses, heterotrophic
bacteria, and protists all play a part in the fate of this fixed carbon. The balance of their activi
ties throughout the water column determines the proportions of fixed carbon that are reminer
alized to CO2, transferred to higher trophic levels, or reach the seafloor. The discovery of this
mechanism, termed the microbial loop, was one of the most important conceptual advances in
biological oceanography, and its significance is considered further in Chapter 8. The sinking
rate of marine snow particles depends greatly in their composition—one area of considerable
current interest and importance is the extent to which microplastics and microbes can affect the
settlement of particles. This is explored in Box 13.1.
14 Chapter 1
Figure 1.8 Schematic diagram Surface Phytoplankton

showing the microbial processes Free-living microbes colonize
occurring in the formation and fate plume of DOM leaching
of a marine snow particle as it falls from sinking particle Metazoan
through the water column. The zooplankton
action of extracellular enzymes and
viral lysis leads to the release of dis- Grazing
solved organic material (DOM).
Bacteria, protists
Chemotaxis
Cellular detritus,
CO2
fecal pellets
Bacterial and
Mucus
protist
assemblages
within particle
Grazing
HOW DID
? CHERNOBYL FALLOUT
HELP THE STUDY OF
Deep ocean Metazoan
zooplankton
MARINE SNOW?
In 1986, a major environmental The sea surface is covered by a gelatinous biofilm
catastrophe occurred when the
nuclear reactor in Chernobyl, The interface between the sea surface and the atmosphere is the site of the exchange of gases,
Ukraine exploded, releasing hun- aerosols and trace elements, in both directions Figure 1.9). We know now that the sea surface
dreds of tons of radioactive par- microlayer (SML, typically up to 1 mm thick) has very different physicochemical and micro-
ticles. These were carried by wind bial composition from the underlying seawater. It contains high concentrations of lipids,
to many distant regions and settled proteins, and polysaccharides, much of it aggregated into TEPs, formed mainly from phy-
with rain on land and sea. Fowler toplankton as described above. The organisms associated with this surface layer are known
et al. (1987) were able to extract
as the neuston. Analysis of the microbial community of the SML shows that the bacterial
some benefit from this tragedy.
community composition contains distinct taxa, but these are interconnected to those in bulk
They had set up sediment traps
to measure vertical transport in seawater below. Surface wind, exposure to UV irradiation, deposition of air-borne dust, and
the Mediterranean Sea. Following other factors are important in determining the composition of the bacterioneuston, and these
the Chernobyl fallout, they found vary greatly according to location. The composition of the phytoneuston—microalgae found
that the pulse of radioactivity— in the SML—is also very different from the phytoplankton, especially in the diversity of
especially the rare nuclides 141Ce diatoms. Recently, fungi have been shown to be a significant component of the SML (p.187).
and 144Ce—was transported to The physical properties of the sea surface are altered by the presence of the SML through the
depths of over 200 m within a few production of surfactants, which modify phenomena such as turbulence and the formation of
days at a rate of 29 m per day. bubbles and micro-waves. This is often visible in the form of surface slicks of calmer water.
Physical processes alone could not This affects the transfer of microbes and organic compounds into the atmosphere via aerosols
account for such rapid settlement.
produced by wind action, which is linked to the formation of clouds and ice, affecting local
Fowler and colleagues concluded
that zooplankton were ingesting
and global climatic conditions (Figure 1.9). This topic is explored further in Chapter 9.
radioactive particles adsorbed to
their food source and repackaging
them as larger, denser particles in SEDIMENTS AND SURFACES
fecal pellets that aggregated with
marine snow to sink at a high rate. Microbes play a major role in marine sediments
Subsequent studies have shown
that the fecal pellets of different More than 70% of the Earth’s surface is covered by marine sediments. On the continental
zooplankton species vary greatly in shelf, sediments are formed due to the accumulation of eroded materials transported into the
their density and sinking rate. ocean as particles of mud, sand, or gravel, together with copious particulate organic matter,
Figure 1.9 Conceptual view of the

processes determining transport
across the sea surface microlayer
(SML). Reprinted from Engel et al.
(2017), CC-BY 3.0.
carbonate- and silica-rich compounds produced by biological activity. The mineral compo
sition reflects the nature of the rocks and the type of weathering. Large rivers such as the
Amazon, Orinoco, or Ganges transfer millions of tons of fine sediments to the ocean each
year. Most of this mud settles along the continental margins or is funneled as dilute suspen
sions by submarine canyons. Here, the sediments may be more than 10 km thick. By con
trast, in much of the Atlantic and Pacific Oceans underneath the ocean gyres, the sediments
may only be 100–1000 m thick. Here, far from the continental land masses, abyssal clays are
formed by the deposition of fine sediments from the continents mixed with wind-blown dust,
volcanic ash, and cosmogenic dust from meteor impact. These accumulate very slowly—less
than 1 mm per 1000 years—while biogenous oozes accumulate at up to 4 cm per 1000 years.
Biogenous oozes contain over 30% of material of biological origin, mainly shells of protistan HOW MANY
plankton, mixed with clay. Oozes are usually insignificant in the shallow waters near conti
nents. Calcareous oozes or muds cover nearly 50% of the ocean floor, especially in the Indian
? MICROBES ARE ON
A GRAIN OF SAND?
and Atlantic Oceans. They are formed by the deposition of the calcium carbonate shells (tests)
of two main types of protist: the coccolithophorids and the foraminifera (see Chapter 6). To answer this question, Probandt
et al. (2018) developed a method
Siliceous oozes are formed from the shells (frustules) of diatoms and radiolarians, which are
to examine individual grains of
composed of opaline silica (SiO2.nH2O). The rate of accumulation of biogenous oozes depends sand from a coastal sediment using
on the rate of production of organisms in the plankton, the rate of destruction during descent to fluorescent in situ hybridization
the seafloor, and the extent to which they are diluted by mixing with other sediments. (FISH) and confocal microscopy,
together with polymerase chain
In the case of coccolithophorids and foraminifera, depth has an important effect on reaction (PCR) amplification of
dissolution of the calcified scales or shells. At relatively high temperatures near the rRNA genes (see Chapter 2 for
surface, seawater is saturated with CaCO3. As calcareous shells sink, CaCO3 becomes methods). They found that indi-
more soluble as a result of the increased content of CO2 in water at lower temperatures vidual grains (just 202–635 µm
and higher pressures. The carbonate compensation depth is the depth at which carbon diameter) were colonized by a
highly diverse community of 104 –
ate input from the surface waters is balanced by dissolution in deep waters; this varies
105 microbes (mostly bacteria, with
between 3000 m in polar waters and 5000 m in tropical waters. For this reason, calcare
smaller numbers of archaea and a
ous oozes tend not to form in waters more than 5000 m deep. Similarly, not all of the few eukaryotes), densely packed in
silica in the frustules of diatoms reaches the ocean floor because bacterial action has a thin film in the indentations on
been shown to play a large part in the dissolution of diatom shells during their descent the sand grain. The wide range of
(p.182). The rate of deposition of protist remains to the seabed is much more rapid than taxa and functional groups found
would be assumed from their small size. This is because they are aggregated into larger shows that the variable physical
particles through egestion as fecal pellets after grazing by zooplankton and through the conditions and nutrient availability
formation of marine snow as described above. In shallower waters near the continen in these grains of surface sediment
tal shelf, the high input of terrigenous sediments mixes with and dilutes sediments of clearly provide the right microen-
biogenous origin. vironments for many of the major
metabolic transformations carried
out by different microbial groups—
There is increasing recognition of the importance of microbial activities in the sediment– a microbial zoo on a tiny grain
water interface (SWI) and deep-sea benthic boundary layer (BBL), which is a layer of homo of sand!
geneous water 10 m or more thick, adjacent to the sediment surface. The SWI includes high
16 Chapter 1
concentrations of particulate organic debris and dissolved organic compounds that become
adsorbed onto mineral particles.
In nutrient-rich areas with high rates of microbial activity, oxygen may be present in only the
top few millimeters or few centimeters of the sediment, but the structure and composition
of the microbial habitat is modified by benthic “storms” and the action of animals such as
worms and burrowing shrimps, which move and resuspend sediments, transporting oxygen
into deeper layers (bioturbation).
As well as the constant “snowfall” of plankton-derived material, concentrated nutrient inputs

reach the seabed in the form of large animal carcasses. For example, time-lapse photography
has shown how quickly fallen whale carcasses attract colonies of animals, and microbiologi
cal studies accompanying these investigations have yielded novel bacteria, some with bio
technological applications (p.390). The microbial communities and symbioses that develop
are similar to those found at hydrothermal vents and cold seeps. Other types of sediment that
provide special habitats for microbes include those in salt marshes, mangroves, and coral
reefs.
Studies of the extent to which carbon fixed in the photic zone finds its way to the seabed, and
its fate in sediments, are important in understanding the role of the oceans in the planetary
carbon cycle. Microbial processes such as production and oxidation of methane and oxidation
and reduction of sulfur compounds are of special interest. Studies of the diversity and activ
ity of microbial life in the various types of sediment are yielding many new insights, mainly
because of the application of molecular techniques, and these are described in subsequent
chapters.
Deep marine sediments contain a vast

reservoir of ancient microbes
The microbiology of deep marine sediments and subsurface rocks is an area of current active
investigation using deep-core drilling and novel coring devices, and microbes have been
detected to a depth of 1.6 km in porous layers that were laid down as sediments tens or hun
dreds of million years ago (MYA). Current estimates of the global distribution of bacteria
and archaea in deep sediments, obtained using a variety of techniques, give a consensus
value of about 3 × 1029 bacterial and archaeal cells. The deep biosphere remains one of the
most inaccessible ecosystems on Earth and investigation is expensive and technologically
challenging, but recent research is providing new insights leading to the conclusion that most
organisms are “barely alive” descendants of cells buried over millions of years, as discussed
in Box 1.1)
Microbes colonize surfaces through

formation of biofilms and mats
In the last few decades, the special phenomena that govern the colonization of surfaces by
microbes have come under intense scrutiny, with the growing recognition that such bio
film formation involves complex physicochemical processes and community interactions.
Biofilms consist of a collection of microbes bound to a solid surface by their extracellular
products, which trap organic and inorganic components. In the marine environment, all kinds
of surfaces including other microbes, plants, animals, sediment particles, rocks, and fabri
cated structures may become colonized by biofilms. Biofilm formation is considered in more
detail in Chapter 3, and its economic importance in biofouling is discussed in Chapter 13.
As a result of metabolic processes, ecological succession can result in the development of

multi-layered structures known as microbial mats. Mats can be several millimeters to a few
centimeters thick. Depending on the nutritional and environmental conditions, mats may
contain multiple types of bacteria, archaea, protists, and fungi (and their viruses) in combina
tion with microbial polymers and sedimentary materials. These are particularly important in
shallow and intertidal waters, but they are also found in deeper nutrient-rich water. The com
position of microbial mats is affected by physical factors such as light, temperature, water
Figure 1.10 Global distribution of

subseafloor sedimentary cell abun-
dance. A. Sedimentation rate. B.
Distance from shore. C. Integrated
number of cells. Reprinted from
Kallmeyer et al. (2012) with per-
mission from National Academy of
Sciences.
content, and flow rate; and by chemical factors such as pH, redox potential, the concentration
of molecular oxygen, sulfide, nitrate, iron, and dissolved organic compounds. Phototrophic
bacteria and diatoms are major components of stratified microbial mats in the photic zone,
and the species composition and zonation are determined by the intensity and wavelength
of light penetration into the mat. Light normally only penetrates about 1 mm into the mat
and anoxic conditions develop below this. The formation and diurnal variations of physico
chemical gradients (especially of oxygen and sulfide) have a major effect on the distribution
of organisms in the mat. Microbial mats formed by chemosynthetic bacteria are common at
hydrothermal vents (Figure 1.12A).
Stromatolites are formed by the trapping of sedimentary particles, cemented together by

microbial exudates to form reefs or pillar-like structures. Fossils of stromatolites are common
in ancient rocks (Figure 1.12B). Cyanobacteria are active on the surface of the structures and
the underlying material is formed by a slow build-up of lithified remains of the former growth
(<1 mm per year). They occur today in a few shallow marine lagoons, such as Shark Bay in
Western Australia (Figure 1.12C).
18 Chapter 1
BOX 1.1 RESEARCH FOCUS
Deep subsurface microbes—are they dead, dormant, or just staying alive?
Studying deep subsurface sediments. Ensuring that samples are to explain the long-term maintenance of microbes in the sediments
recovered without contamination during drilling is a major chal- over millions of years. They concluded that the organisms in the deep
lenge, depending on multi-national consortia of microbiologists, oligotrophic sediments survive by using the low available energy to
geologists, and chemists, such as the Integrated Ocean Discovery just “staying alive,” rather than growing and reproducing. The rate
Programme (IODP) (Hoehler and Jørgensen, 2013) operating spe- of respiration in these deep sediments was found to be about 104
cialized drilling ships (Figure 1.11). Based on analysis of various times lower than at the seafloor and the density of organisms is only
studies using epifluorescence counts, Whitman et al. (1998) esti- about 100–1000 cells cm−3. Jørgensen (2011) estimates that cells with
mated of the number of bacteria and archaeal cells in the deep such a low metabolic rate might reproduce only once every several
marine subsurface sediments at 3.5 × 1030 bacterial and archaeal thousand years. One possibility is that cells in this nutrient-deprived,
cells. More recent calculations put the figure about ten times lower, semi-solid environment are not subject to predation by protists or
with an estimated biomass of 10 Gt (Pg) carbon (Bar-On et al., attack by viruses and this enables a stable population to exist, with
2018). What are all these organisms doing—are they dead, dor- cells devoting all their metabolic efforts to maintenance (turnover
mant, or alive? Different investigators have produced conflicting and repair of essential cell components like DNA, proteins, and
opinions on this issue (reviewed by Orcutt et al., 2013). membrane lipids) rather than growth and reproduction.
In ocean regions with high productivity, oxygen becomes quickly Could such cells be stimulated into a more active lifestyle? In
depleted below the seafloor and the anaerobic reduction of sulfate experiments conducted by Morono et al. (2011), deep sediments
coupled to the oxidation of organic matter is the dominant metabolic from beneath the Japan sea were incubated with isotope-labeled
process in sediments. However, under the extremely oligotrophic nutrients such as glucose or amino acids. They found that most of
subtropical ocean gyres, the rate of deposition of organic material the cells incorporated these nutrients, increasing their metabolic
reaching the seabed is so low (a few millimeters every 1000 years) rate 1000 times. This could be explained if most of the cells are
that oxygen can penetrate far below the seafloor (Røy et al., 2012). in a truly dormant state, such as endospores that become activated
The amount of energy available to sustain life under these conditions into vegetative growth by the addition of nutrients. This is known
is very limited. Bradley et al. (2019) developed a mathematical model to occur in laboratory studies of endospores. Although endospores
are found in deep sediments and could survive long periods of
environmental stress such as starvation, Jørgensen (2011) argues
that the amount of energy needed to germinate and return to an
active growth state far exceeds that found in these deeply buried,
ancient sediments. Trembath-Reichert et al. (2017) analyzed mate-
rial recovered from a coal seam 2.5 km below the seabed off the
coast of Japan. In this deep sample, the tiny microbial cells were
very scarce (10–100 cm−3) and DNA sequence analysis showed that
the bacterial community composition was more closely related to
that found in forest soil than in marine sediments. This indicates
that they originate from rich organic material from primeval forests
that was buried by subsidence into the ocean over 20 million years
ago and subsequently overlaid by 2 km thick shales. Studies of the
diversity of deep subsurface communities are still rather limited,
although metagenomic analyses are beginning to yield valuable
information. Based on studies of distinctive membrane lipids, sup-
ported by nucleic acid-based techniques, in sediments more than 1
m deep, it appears that archaea constitute a much greater proportion
of the biomass than bacteria (Lipp et al. 2008). Archaea may have a
selective advantage due to the nature of their cell membranes.
Do populations of these buried microbes adapt to the new

low-nutrient conditions by evolving? To answer this question,
Starnawski et al. (2017) investigated the assembly and evolution
of microbial communities in 8700-year-old 10 m thick sediments
in Arhus Bay, Denmark. They used DNA sequencing techniques
to show that a small number of specific bacterial types were pres-
Figure 1.11 A. The ocean drilling vessel JOIDES Resolution. ent throughout all sample depths. This subset represented a small
B. Sampling a sediment core for microbial analysis. Credit: proportion of the diversity near the surface but made up 40–50%
William Crawford, Integrated Ocean Drilling Program, US of the total microbial community in the deeper layers. The authors
Implementing Organization.
concluded that rare members of surface sediment microbial commu- concluded that as populations were separated over time (thousands)
nities become predominant as they become buried over thousands of years and space (tens of meters) during burial, there was hardly
of years. By comparing the whole genome sequences obtained from any accumulation of mutations. Given the extremely low generation
single cells from different depths, they showed that their genetic times of cells due to low-nutrient availability, they suggested that
diversification is minimal. Since the stable structure of the sedi- their findings can be generalized to the deepest sediments, which
ments prevents exchange of cells or genes, Starnawski et al. (2017) are millions of years old.
SOME EXAMPLES OF SPECIAL HABITATS—THE MICROBIAL MATS

DEEP SEA, POLAR OCEANS, CORAL i AND EVOLUTION
REEFS, AND LIVING ORGANISMS Some of Earth’s oldest sedimentary
rocks in Western Australia contain
Microbial activity at hydrothermal vents evidence of complex microbial
communities that existed 3.48
fuels an oasis of life in the deep sea billion years ago (BYA). These
Hydrothermal vents form a specialized and highly significant habitat for microbes. They fossilized microbially induced
occur mainly at the mid-ocean ridges at the boundary of the Earth’s tectonic plates, where sedimentary structures (MISS) and
seafloor spreading and formation of new ocean crust is occurring (Figure 1.13A). Over 300 stromatolites are believed to have
formed from mats colonizing an
such sites have been studied in the Pacific and Atlantic Oceans and many others are pre-
ancient shoreline or lagoon and
dicted on the basis of geological surveys. Seawater permeates through cracks and fissures
consist of layers of sediment and
in the crust and interacts with the heated underlying rocks, thereby changing the chemical organic material (Noffke et al.,
and physical characteristics of both the seawater and the rock. The permeability structure 2013). These ancient MISS prob-
of the ocean crust and the location of the heat source determine the circulation patterns of ably contained anaerobic photo-
hydrothermal fluids. As cold seawater penetrates into the ocean crust, it is gradually heated trophic bacteria. Cyanobacteria
along its flow path, leading to the removal of magnesium from the fluid into the rock, with evolved subsequently (~3 BYA),
production of acid during the process. This leads to the leaching of other major elements and and this led to the development
transition metals from the rock into the hydrothermal fluid, and sulfate in the seawater is of an oxygen-containing atmo-
removed by precipitation and reduction to hydrogen sulfide. As the percolating fluids reach sphere. This heralded the evolu-
tion of eukaryotic organisms (~2
the proximity of the magma heat source, extensive chemical reactions occur within the rock
BYA) and eventually, multicellular
and the pressurized fluids are heated to over 350°C, becoming buoyant and rising toward the
life (0.6 BYA). Until the start of
ocean floor. As they rise, decompression causes the fluids to cool slightly, and precipitation the Cambrian period (~0.54 BYA),
of metal sulfides and other compounds occurs en route. The hydrothermal fluid is injected microbial mats are believed to have
dominated the surface of the ocean
floor, but this is thought to have
ended with the diversification of
animals that began burrowing into
the seabed.
Figure 1.12 A. Chemosynthetic

microbial mats covering red algae
and coral in an area where hydro-
thermal vent and coral reef com-
munities overlap at 190 m depth. B.
Cross section of stromatolite fossil
(Eocene period, 56–34 MYA) from
Fort Laclede Bed, Wyoming showing
layered structure due to microbial
growth and sediment accumula-
tion. C. Stromatolites at the hyper-
saline Hamelin Pool, Shark Bay, W.
Australia. Credits: A. Submarine
Ring of Fire 2004 Exploration,
NOAA Vents Program; B. James St.
John, CC-BY-SA-2.0 via Wikimedia
Commons; C. Bryn Pnzauger. CC BY
2.0 via Wikimedia Commons.
20 Chapter 1
Figure 1.13 A. Schematic diagram

of processes occurring at hydro- Seawater Plume of superheated vent
thermal vent systems. Gradients of enters
and manganese oxides and
temperature and chemical elements ocean crust silicates precipitate in seawater
create a variety of habitats for diverse
microbial and animal communities. 350°C
B. A venting black smoker emit-
“Smoker” chimney
ting jets of particles of iron sulfide. formed by massive
Image shows a dense colony of Riftia Sedimentation
preciptation of
pachyptila giant tubeworms. Credit:
NOAA Pacific Marine Environmental Plume at warm vent
Laboratory. 6–23°C Seawater 2–4°C
Shallow rocks
10–200 m (20–100°C )
Permeat ion Deep rocks

1–3 km (> 350°C) enriched with Cu,
Mn, Fe, Zn, S, Si
Magma heat source
A.
B.
into the ocean as plumes of mineral-rich superheated water. The hottest plumes (up to 350°C)
are generally black, because of the high content of metal sulfide and sulfate particles, and
precipitation occurs as the hot plume mixes with the cold seawater. Some of these precipitates
form chimney structures called “black smokers” (Figure 1.13B) while others are dispersed
through the water and form sediments in the vicinity. In other parts of the vent field, the cir-
culation of hydrothermal fluid may be shallower, leading to diffuse plumes of water heated
to 6–23°C. The gradients of temperature and nutrients that exist at hydrothermal systems
provide a great diversity of habitats for microbes suspended in the surrounding heated waters,
in sediments, and attached to surfaces of the chimneys. Many of these are hyperthermo-
philic bacteria and archaea, which can grow at temperatures up to 121°C, while others grow
at lower temperatures further from the fluid emissions. Molecular studies are revealing an
astonishing diversity of such organisms, many of which have biotechnological applications.

HOW VULNERABLE
The microbiology of the deep subsurface rocks beneath vents is also now under investigation,
and many novel microbes and metabolic processes are being discovered. Microbial activity ? ARE VENT
COMMUNITIES?
in the deep subsurface contributes to the chemical changes in composition during circulation
of the hydrothermal fluids. Hydrothermal vent communities
are among the most productive
Hydrothermal vent systems were first described in 1977, when scientists aboard the submers ecosystems on Earth, but they
ible Alvin, from Woods Hole Oceanographic Institution, were exploring the seabed about cover a relatively small area and
2500 m deep near the Galapagos Islands. The discovery of life around the vents was totally are very ephemeral, lasting only
months or a few years. The flow of
unexpected. The Alvin scientists observed dense communities of previously unknown ani
vent fluids may gradually decline,
mals, including giant tubeworms, clams, anemones, crabs, and many others. Subsequent
or volcanic eruptions may destroy
research showed that the warm waters near hydrothermal vents contain large populations the site completely. The key ani-
of chemosynthetic bacteria and archaea, which fix CO2 using energy from the oxidation of mals inhabiting these sites depend
sulfides in the vent fluids. This metabolism supports a food chain with many trophic levels on production of large quantities
that is independent of photosynthesis. We now know that many of the animals at vent sites of larvae with sufficiently long
contain chemosynthetic bacteria as symbionts within their tissues or on their surfaces—these lifespans for them to be dispersed
relationships are discussed in Chapter 10. In addition, bacterial populations directly support via currents until a new vent site
the growth of filter-feeding animals, such as clams and mussels, or shrimp that graze on is located. Goffredi et al. (2017)
microbial mats. Previously, animal life was thought always to rely ultimately on the fixation showed that differences in the
of CO2 by photosynthesis, but the vent communities function without the input of material overlying sediment and the chem-
istry of vent fluids can result in
derived from the use of light energy, although the sulfide oxidation depends on dissolved
colonization of neighboring vents
oxygen in the water, and the origin of this is photosynthetic. by very different animal species.
Vent ecosystems clearly show resil-
ience to natural disturbance but
Cold seeps also support diverse life may be threatened by undersea
based on chemosynthesis mining for rare minerals deposited
around vents unless effective con-
Cold seeps are abundant along the continental shelf and slope, where the upwards percola servation measures are put in place
tion of fluids through fissures in the sediments is caused by plate tectonic activity and other (Van Dover, 2014).
geological processes, allowing high concentrations of hydrocarbons to seep into the water
column. The temperature of emissions is the same as ambient seawater, or just a little higher,
but they were described as “cold” seeps to distinguish them from the warm and superheated
hydrothermal vents. Cold seeps were first discovered in 1983 in the Gulf of Mexico at a depth
of 3.2 km and have subsequently been found in many other regions. They are most common
along the continental margins, and although they usually occur in deep water (the deepest is
at 7.3 km in the Japan Trench), there are some shallow seeps off the coasts of Chile, northern
California, Oregon, and Denmark.
Methane is produced in anoxic sediments by a range of methanogenic archaea (p.87), and in

very deep sediments it is formed by through thermogenic chemical transformation of organic
matter at high pressure and temperature. Methane has a low density and rises to stability
zones with a specific combination of temperature and pressure under the seabed, where it
combines with water molecules combine to form a stable crystalline structure (clathrate).
Seeps are formed when fissures occur, destabilizing the clathrate due to changes in tempera
ture or pressure. Some sites are associated with seeps of hypersaline brines or leakage of oil
or gas from hydrocarbons reservoirs. The methane supports prolific chemosynthetic com
munities consisting of free-living methanotrophic bacteria and archaea, as well as those liv
ing symbiotically with invertebrates, including bivalve mollusks from five different families
and siboglinid tubeworms (Chapter 10). Reef-like structures are created by the deposition of
calcium carbonate as a product of the anaerobic oxidation of methane (p.89) by consortia of
methanotrophic archaea and sulfate-reducing and bacteria. A wide range of other animals
including polychaete worms, sea stars, urchins, echinoderms, gastropods, crabs and lobsters,
and shrimp are sustained by this chemosynthetic community (Figure 1.14).
Microbes inhabit the interface of

brine pools in the deep sea
Distinct pools of hypersaline water occur in the Gulf of Mexico, Red Sea, and Eastern
Mediterranean Sea, created by movement of the Earth’s crust. For example, those in the
Mediterranean Sea are thought to have been formed when a large area of the sea became
22 Chapter 1
isolated from the Atlantic Ocean about 250 MYA. Regions of the sea evaporated, leaving a
i
LISTENING IN TO
layer of rock salt, which later became covered by sediments after the Mediterranean basin
METHANE SEEPS
reflooded. Movement of the tectonic plates has exposed the salt deposits in a few areas. Here,
To date, most methane seeps the salts have dissolved to form dense pockets of highly concentrated solutions of different
have been discovered via under- salts, separated from the overlying seawater by extremely sharp density gradients (pycno
water exploration using manned clines) and environmental interfaces (chemoclines). These undersea brine pools have extreme
submersibles or remotely oper- physical and chemical conditions, notably the complete lack of oxygen and near-saturated
ated underwater vehicles (ROVs, solutions of salts (up to ten times the salinity of seawater). They are therefore termed Deep
p.32). Scientists recently detected
Sea, Hypersaline, Anoxic Basins (DHABs).
nearly 1000 seeps about 16 km
off the coast of Oregon by using a
hydrophone to record the sound
The interface is just a few meters thick, and accurate sampling within this chemocline at
of methane bubbles escaping from such a great depth requires great ingenuity. Conventional remotely operated vehicles (ROVs)
the seabed. Dziak et al. (2018) and manned submersibles cannot be used because of the damaging properties of the brines.
found that the frequency of the Because of the extreme conditions, organisms growing in such habitats require special adap
sound emitted is related to the size tations, and it might be expected that the diversity of microbial types would be low. However,
of the gas bubble. The next step through the use of DNA-based identification methods, many previously unknown taxa of bac
will be to fine-tune the detec- teria have been identified, occupying narrow niches in the highly stratified interface. Archaea
tion process, so that hydrophone appear to be less prevalent than bacteria. The low availability of organic compounds at such
methods can be used directly to depths suggests that chemoautotrophic metabolism sustains these communities and there is
estimate the size of the methane
evidence for production of methane and sulfur cycling. Eukaryotic microbes (heterotrophic
reservoirs.
protists) are also abundant at the interface, and there is extensive grazing of the bacteria. It
appears that some protists may be protected from the extreme anoxic and sulfidic chemical
conditions by symbiotic interactions or partnerships with bacteria. Each basin seems to be
inhabited by a distinctive set of microbial species, which have adapted through evolution to
the unique chemical conditions of each DHAB.
At the edge of some brine pools, there are communities of mussels containing chemosyn
thetic bacteria and associated invertebrates, similar to those found at methane seeps.
Microbes in sea ice form an important part

of the food web in polar regions
At the poles, the temperature is so low during the winter that large areas of seawater freeze to
form sea ice, some of which forms adjacent to the coastal shoreline and some of which forms
floating masses of pack ice. Sea ice forms when the temperature is less than −1.9°C, the freez
ing point of water at 35‰ salinity. The first stage in sea-ice formation is the accumulation of
minute crystals of frazil ice on the surface, which are driven by wind and wave action into
aggregated clumps called grease ice. These turn into pancake-shaped ice floes that freeze
together and form a solid ice cover. At the winter maxima, the combined coverage by sea ice
at the north and south polar regions is almost 10% of the Earth’s surface (1.8 × 107 km2 in
the Antarctic and 1.5 × 107 km2 in the Arctic). During the formation of frazil ice, planktonic
microbes become trapped between the ice crystals and wave motion transports more organ
isms into the grease ice during its formation. Near the ice-air interface, temperatures may be
Figure 1.14 Mussels and shrimp at

a chemosynthetic cold-seep com-
munity, Gulf of Mexico. Credit:
NOAA-OE, Expedition to the Deep
Slope 2007.
as low as −20°C during the depths of the polar winter, while the temperature at the ice-water
interface remains fairly constant at about −2°C. When seawater freezes, it forms a crystal
line lattice of pure water, excluding salts from the crystal structure. The salinity of the liquid
phase increases, and its freezing point drops still further. This very cold, high-density, high-
salinity (up to 150‰) water forms brine pockets or channels within the ice, which can remain
liquid to −35°C. The ice becomes less dense than seawater and rises above sea level, with the
channels draining brine through the ice to the underlying seawater. Thus, sea ice is very dif
ferent from freshwater glacial ice. Loss of sea ice cover is a topic of great concern (Box 1.2).
The structure of sea ice provides a labyrinth of different microhabitats for microbes, with varia
tions in temperature, salinity, nutrient concentration, and light penetration. This enables coloni
zation and active metabolism by distinctive mixed communities of cold-adapted (psychrophilic)
photosynthetic and heterotrophic protists and bacteria, as well as viruses. Microbial activities
also alter the physicochemical conditions, mainly owing to the production of large amounts
of cryoprotectant compounds and extracellular polymers, leading to the creation of additional
microenvironments. The dominant photosynthetic organisms near the ice–sea interface are pen
nate diatoms and small dinoflagellates (Figure 1.15A). The density of diatoms in sea ice may be
up to 1000 times that in surface waters. Through photosynthesis, the microalgae make a small,
but significant, contribution to primary productivity in the polar regions. For example, the con
tribution of sea ice to primary productivity in the Southern Ocean is only about 5% of the total,
but it extends the short summer period of primary production and provides a concentrated food
source that sustains the food web during the winter. During the Antarctic winter, microalgae on
the undersurface of sea ice are the main source of food for grazing krill, shrimp-like crustaceans
that are the main diet of fish, birds, and mammals in the Southern Ocean. A wide range of pro
tists and heterotrophic bacteria have been found in sea ice, including new species with biotechno
logical potential. Some microbes remain active—albeit at a much-reduced metabolic rate—even
in the coldest parts of the ice and in “frost flowers” formed on the surface of the ice, where they
are trapped in pockets of very low temperatures and high-salinity (Figure 1.15B).
Figure 1.15 (a) Light microscopy

image of diatoms living in annual
sea ice, McMurdo Sound, Antarctica.
(b) Frost flowers over young sea ice
in the central Arctic Ocean. Credits:
(a) Gordon T. Taylor, NOAA Corps
Collection. (b) Matthias Wietz, MPI
Marine Microbiology, Bremen.
24 Chapter 1
What will happen when the sea-ice melts?
Global warming is affecting polar regions more rapidly than trophic levels. Thus, an increase in small Synechococcus in place
any other parts of the planet. Although there is a large natural of larger phytoplankton in a warmer Arctic Ocean could have major
annual variation in the thickness and extent of summer sea ice in the effects on transfer of productivity to other organisms.
Arctic Ocean, these have shown a dramatic decline since the 1970s.
In 2018, some of the thickest and oldest areas of ice to the north of Benthic microbes are also affected. Antje Boetius and colleagues
Greenland started to break up (Figure 1.16). Notz and Stroeve (2016) at the Alfred Wegener Institute and Max Planck Institute of Marine
provide compelling evidence that this is directly linked to CO2 emis- Microbiology are undertaking an intensive research program to inves-
sions as a result of human activity, and their models predict that the tigate the microbiology of current and archived samples of Arctic
Arctic Ocean will be free of summer ice by the end of this century. deep-sea sediments, revealing important information about changes
The loss of ice cover results in changes to wind patterns and warmer in microbial diversity and how the flux of particulate organic mat-
and less saline waters in the upper ocean. Also, we now know that ter is affected by the loss of permanent ice cover. Rapp et al. (2018)
sea ice absorbs large amounts of CO2 from the atmosphere (Søgaard report the analysis of microbial communities in areas affected by the
et al., 2013). Most significantly, loss of summer ice also reduces the summer ice melt in 2012, which was the largest decline to date. Vast
albedo effect resulting in a positive feedback, which increases the quantities of ice algae associated with the underside of the sea ice
absorption of solar energy by seawater rather than reflecting sun- became detached and sank to the seafloor at over 4000 m in depth.
light. This further accelerates the rise in temperature. Many scien- Using high-throughput DNA sequencing, Rapp and colleagues stud-
tific programmes are investigating the impact of these changes and ied the diversity of different groups of microbes in the sea ice, in
microbiological research is especially important. We urgently need melt water and in the surface sediment beneath the melting ice. The
to know how changes in microbial communities and their activities sea-ice algae aggregates were shown to be mostly composed of dia-
are altering the cycling of carbon and other elements. toms, especially Melosira arctica. The large filaments of this diatom
sank rapidly to the seabed. The sinking aggregates were shown to
Changes in Arctic picophytoplankton. One example of change transport bacteria such as Flavobacteriia and Gammaproteobacteria,
has been observed in apparent shifts of picophytoplankton diversity including Glaciecola and Paraglaciecola. These are known to be
in the Arctic Ocean. Paulsen et al. (2016) found high numbers of the actively involved in the breakdown of algal and other organic mate-
cyanobacterium Synechococcus at high latitudes. This was surpris- rial via the production of extracellular enzymes. Labyrinthulids were
ing, as Arctic water masses are usually thought to be dominated also detected—these protists are known to be active in degradation
by larger picoeukaryotes adapted to low temperatures, such as of algae (p.183). Rapp et al. found that the algal deposits changed
Micromonas spp. This could be attributed in part to a change in the the community composition on the seafloor by introducing bacteria
flow of water from the Atlantic into the Arctic Ocean due to global from the sea ice, although these appeared to be overgrown by spe-
warming, but analysis of the distribution of different genetic clades cific groups of indigenous deep-sea bacteria within a few months.
of the cyanobacteria suggests that some of them have adapted to If strong summer ice melting becomes a regular occurrence as pre-
Arctic conditions. Because populations of Synechococcus are con- dicted, the abrupt export of large amounts of sea-ice algae and asso-
trolled by grazing by small heterotrophic protists, Paulsen and col- ciated microbiota will become more frequent. The authors suggest
leagues concluded that much of their biomass would be recycled that this could lead to permanent changes in bacterial community
within the microbial loop (p.220), rather than transferring to higher composition, which may lead to significant changes in the cycling of
nutrients in the surface sediments.
Changes in Antarctic food webs. Warming is also occurring in

the Antarctic, where increased melting of the ice-sheets increases
the input of fresh water, altering the salinity and structure of the
surrounding water column. Consequent changes in ocean food web
structures will also affect benthic communities, as seasonal shifts
in different types of phytoplankton in the water column or underside
of sea ice will affect the flow of fixed carbon to the seafloor. Based
on a large-scale study of microbial diversity in Antarctic sediments,
Learman et al. (2016) found that community composition varied
greatly with geographic location and was strongly influenced by
the nature of organic matter reaching the seafloor. Warming could
lead to an increase in meltwater, stimulating increased phytoplank-
ton blooms transporting organic matter to the seabed. Learman and
Figure 1.16 Time series showing the Arctic ice remain- colleagues suggest that this might cause a shift from communi-
ing at the end each summer melt season since 1985. The ties dominated by lithotrophic organisms (such as some types of
area of the oldest ice has declined 16-fold. Credit: M. archaea) to a greater proportion of chemoheterotrophs. This could
Tschudi, S. Stewart, University of Colorado, and W. Meier, cause significant changes to biogeochemical cycling.
J. Stroeve, NSIDC.
Microbial activity underpins productive

food webs in coral reefs
The most familiar coral reefs are those found in the shallow photic zone, especially in tropi-
cal and subtropical areas. These present specialized habitats, in which symbiotic interactions
between corals and microbes are responsible for primary production. Symbiotic dinoflagel-
lates (zooxanthellae) are responsible for the fixation of CO2, which promotes growth of the
coral animal tissue and skeleton, but also leads to large excesses of fixed carbon that fuels
microbial processes in the seawater and sediments surrounding the reef. Corals produce large
amounts of mucus, much of which forms TEPs and gels which provide a major source of
nutrients sustaining the growth of planktonic bacteria or aggregate to form sinking particles
which fuel benthic activities. Thus, although coral reefs only occupy about 0.1% of the sea-
floor area and occur in ocean areas of generally low productivity (due to lack of nutrient
input), they are as productive as tropical rain forests and are estimated to contain a third of
all marine species. Recent studies have shown that many other microbes associated with cor-
als and other reef organisms are involved in the primary production and recycling of carbon,
nitrogen, and other key elements. We now recognize that major phase shifts in microbial
activity are responsible for the degradation of coral reefs, with profound implications for
marine life and the destabilization of safety and livelihood of millions of people. Climate
change is a major threat to the world’s reefs, with severe mass bleaching affecting many
tropical reefs (most notably, Australia’s Great Barrier Reef) in years when average sea sur-
face temperatures have been just 1°C or so above normal. As sea levels rise, reefs may not be
able to grow quickly enough to maintain optimum light levels, while ocean acidification will
reduce their ability to calcify. These issues are discussed in detail in Chapter 10.
Living organisms are the habitats of many microbes

Microbial biofilms also form on the surfaces of all kinds of animals, seaweeds, and coastal plants;
these provide a highly nutritive environment through secretion or leaching of organic compounds.
Many organisms seem selectively to enhance surface colonization by certain microbes and dis-
courage colonization by others. This may occur by the production of specific compounds that
inhibit attachment or growth of certain microbes. Once established, particular microbes may
themselves influence colonization by other types. These processes offer obvious applications in
the control of biofouling (p.356). As well as surface (epibiotic) associations, microorganisms can
form endosymbiotic associations within the body cavities, tissue, or cells of living organisms.
Many microalgae (such as diatoms, dinoflagellates, and prymnesiophytes) and other pro-
tists (such as ciliates) harbor bacteria on their surfaces, or as endosymbionts within their
cells (Figure 4.11). Intimate associations between bacterial and archaeal cells are also being
revealed by new imaging techniques (Figure 5.5). Seaweeds and seagrasses have dense popu-
lations of bacteria (up to 106 per cm2) on their surfaces, although this varies considerably with
species, geographic location, and climatic conditions.
The external surfaces and intestinal content of animals provide a variety of habitats to a wide
diversity of microbes. Such associations commonly lead to some mutual benefit for host and
microbe—examples of symbiotic interactions between animals and microbes are considered
in Chapter 10. Pathogenic interactions may also result—microbial diseases of marine organ-
isms are discussed in Chapter 11.
Conclusions
This chapter has introduced the various types of marine microbes and some of the wide range
of habitats that they occupy. The adaptations of marine microbes to the different physical,
chemical, and biological conditions encountered have led to the evolution of highly diverse
microbes. The discovery that these tiny microbes are present in such large numbers and
biomass—and that they are responsible for the biogeochemical processes that shape our
planet—can be viewed as one of the most important advances of modern science. Subsequent
chapters build on this introduction by exploring the mechanisms underlying this diversity of
form and function.
26 Chapter 1
References and further reading Ocean habitats

Origins and scope of marine microbiology Azam, F. and Long, R. A. (2001). Sea snow microcosms. Nature 414: 495–498.
Azam, F. and Malfatti, F. (2007). Microbial structuring of marine ecosys
Bar-On, Y. M., Phillips, R., and Milo, R. (2018). The biomass distribution
tems. Nat. Rev. Microbiol. 5: 782–791.
on Earth. Proc. Nat. Acad. Sci. 115: 6506–6511.
Costello, M. J. and Breyer, S. (2017). Ocean depths: The mesopelagic and
Brown, J. W. (2015). Principles of Microbial Diversity. ASM Press.
implications for global warming. Curr. Biol. 27: R19–R41.
Caron, D. A., Worden, A. Z., Countway, P. D., et al. (2008). Protists are
Cunliffe, M., Engel, A., Frka, S., et al. (2013). Sea surface microlayers: A
microbes too: A perspective. ISME J. 3: 4–12.
unified physicochemical and biological perspective of the air–ocean inter
Ciccarelli, F. D., Doerks, T., von Mering, C., et al. (2006). Toward auto face. Prog. Oceanog. 109: 104–116.
matic reconstruction of a highly resolved tree of life. Science 312: 697.
Cunliffe, M. and Murrell, J. C. (2009). The sea-surface microlayer is a
Dagan, T. and Martin, W. (2009). Getting a better picture of microbial gelatinous biofilm. ISME J. 3: 1001–1003.
evolution en route to a network of genomes. Phil. Trans. Roy. Soc. B Biol.
Engel, A., Bange, H. W., Cunliffe, M., et al. (2017). The ocean’s vital skin:
Sci. 364: 2187–2196.
Toward an integrated understanding of the sea surface microlayer. Front.
Doolittle, W. F. (1999). Phylogenetic classification and the universal tree. Mar. Sci. 4: 165.
Science 286: 1433.
Fowler, S. W., Buat-Menard, P., Yokoyama, et al. (1987). Rapid removal of
Embley, M. and Williams T. (2016). Only two domains, not three: Chernobyl fallout from Mediterranean surface waters by biological activ
Changing views on the tree of life. Microbiol. Today 2016: 70–73. ity. Nature 329: 56–58.
Forterre, P. (2015). The universal tree of life: An update. Front. Microbiol. Grossart, H. P., Kiorboe, T., Tang, K. W., et al. (2006). Interactions
6: 717. between marine snow and heterotrophic bacteria: Aggregate formation
Gasol, J. M. and Kirchman, D. (2018). Introduction: The evolution of and microbial dynamics. Aquat. Microb. Ecol. 42: 19–26.
microbial ecology of the ocean. In Microbial Ecology of the Oceans, ed. Kjørboe, T. (2001). Formation and fate of marine snow: Small- scale pro
Gasol, J. M. and Kirchman, D. L., pp. 1–46, Wiley Blackwell. cesses with large-scale implications. Sci. Mar. 65: 57–71.
Grossart, H.-P. and Rojas-Jiminez, K. (2016). Aquatic fungi: Targeting the Mühlenbruch, M., Grossart, H. P., Eigemann, F., and Voss, M. (2018).
forgotten in microbial ecology. Curr. Opin. Microbiol. 31: 140–145. Phytoplankton‐derived polysaccharides in the marine environment and their
Henderson, G. P., Gan, L., and Jensen, G. J. (2007). 3-D ultrastructure interactions with heterotrophic bacteria. Environ. Microbiol. 20: 2671–2685.
of O. tauri: Electron cryotomography of an entire eukaryotic cell. PLoS Nissimov, J. I. and Bidle, K. D. (2017). Stress, death, and the biological
ONE 2: e749. glue of sinking matter. J. Phycol. 53: 241–244.
Hug, L. A., Baker, B. J., Anantharaman, K., et al. (2016). A new view of Seymour, J. R. and Stocker, R. (2018). The ocean’s microscale: A microbe’s
the tree of life. Nat. Microbiol. 1: 16048. view of the sea. In Microbial Ecology of the Oceans, ed. Gasol, J. M. and
Karl, D. M. and Proctor, L. M. (2008). Foundations of microbial oceanog Kirchman, D. L., pp. 289–466, Wiley Blackwell.
raphy. Oceanography 20: 16–27. Verde, C., Giordano, D., Bellas, C. M., et al. (2016). Polar marine microor
Keeling, P. J. and de Campo, J. (2017). Marine protists are not just big ganisms and climate change. Adv. Microb. Physiol. 69: 187–215.
bacteria. Curr. Biol. 27: R451–R459. Verdugo, P., Alldredge, A. L., Azam, F., et al. (2004). The oceanic gel
Kolter, R. and Maloy, S. (eds.) (2012). Microbes and Evolution: The World phase: A bridge in the DOM-POM continuum. Mar. Chem. 92: 67–85.
That Darwin Never Saw. ASM Press.
Lawton, G. (2009). Why Darwin was wrong about the tree of life. New Sediments and surfaces
Sci. 2692: 34–39. Betts, H. C., Puttick, M. N., Clark, J. W., et al. (2018). Integrated genomic
Martin, W. and Embley, T. M. (2004). Evolutionary biology: Early evolu and fossil evidence illuminates life’s early evolution and eukaryote origin.
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Nasir, A., Kim, K. M., Da Cunha, V., and Caetano-Anollés, G. (2016). Bolhuis, H., Cretoiu, M. S. and Stal, L. J. (2014). Molecular ecology of
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References
Bar-On, Y. M., Phillips, R., and Milo, R. (2018). The biomass distribution Whitman, W. B., Coleman, D. C., Wiebe, W. J. (1998). Prokaryotes: The
on Earth. Proc. Nat. Acad. Sci. 115: 6506–6511. unseen majority. Proc. Nat. Acad. Sci. USA 95: 6578–6583.
Brown, J. W. (2015). Principles of Microbial Diversity. ASM Press. Yayanos, A. A. (2003). Marine microbiology at Scripps. Oceanography
Caron, D. A., Worden, A. Z., Countway, P. D., et al. (2008). Protists are 16: 63–75.
microbes too: A perspective. ISME J. 3: 4–12. Zhao, X., Schwartz, C. L., Pierson, J., et al. (2017). Three-dimensional
Ciccarelli, F. D., Doerks, T., von Mering, C., et al. (2006). Toward auto structure of the ultraoligotrophic marine bacterium “Candidatus
matic reconstruction of a highly resolved tree of life. Science 312: 697. Pelagibacter ubique”. Appl. Environ. Microbiol. 83: e02807–16.
Dagan, T. and Martin, W. (2009). Getting a better picture of microbial Azam, F. and Long, R. A. (2001). Sea snow microcosms. Nature 414:
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Sci. 364: 2187–2196. Azam, F. and Malfatti, F. (2007). Microbial structuring of marine ecosys
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Science 286: 1433. Costello, M. J. and Breyer, S. (2017). Ocean depths: The mesopelagic and
Embley, M. and Williams T. (2016). Only two domains, not three: implications for global warming. Curr. Biol. 27: R19–R41.
Changing views on the tree of life. Microbiol. Today 2016: 70–73. Cunliffe, M., Engel, A., Frka, S., et al. (2013). Sea surface microlayers:
Forterre, P. (2015). The universal tree of life: An update. Front. Microbiol. A unified physicochemical and biological perspective of the air–ocean
6: 717. interface. Prog. Oceanog. 109: 104–116.
Gasol, J. M. and Kirchman, D. (2018). Introduction: The evolution of Cunliffe, M. and Murrell, J. C. (2009). The sea-surface microlayer is a
microbial ecology of the ocean. In Microbial Ecology of the Oceans, ed. gelatinous biofilm. ISME J. 3: 1001–1003.
Gasol, J. M. and Kirchman, D. L., pp. 1–46, Wiley Blackwell. Engel, A., Bange, H. W., Cunliffe, M., et al. (2017). The ocean’s vital skin:
Grossart, H.-P. and Rojas-Jiminez, K. (2016). Aquatic fungi: Targeting Toward an integrated understanding of the sea surface microlayer. Front.
the forgotten in microbial ecology. Curr. Opin. Microbiol. 31: 140–145. Mar. Sci. 4: 165.
Henderson, G. P., Gan, L., and Jensen, G. J. (2007). 3-D ultrastructure Fowler, S. W., Buat-Menard, P., Yokoyama, et al. (1987). Rapid removal of
of O. tauri: Electron cryotomography of an entire eukaryotic cell. PLoS Chernobyl fallout from Mediterranean surface waters by biological activ
ONE 2: e749. ity. Nature 329: 56–58.
Hug, L. A., Baker, B. J., Anantharaman, K., et al. (2016). A new view of Grossart, H. P., Kiorboe, T., Tang, K. W., et al. (2006). Interactions
the tree of life. Nat. Microbiol. 1: 16048. between marine snow and heterotrophic bacteria: Aggregate formation
and microbial dynamics. Aquat. Microb. Ecol. 42: 19–26.
Karl, D. M. and Proctor, L. M. (2008). Foundations of microbial oceanog
raphy. Oceanography 20: 16–27. Kjørboe, T. (2001). Formation and fate of marine snow: Small- scale pro
cesses with large-scale implications. Sci. Mar. 65: 57–71.
Keeling, P. J. and de Campo, J. (2017). Marine protists are not just big
bacteria. Curr. Biol. 27: R451–R459. Mühlenbruch, M., Grossart, H. P., Eigemann, F., and Voss, M. (2018).
Phytoplankton‐derived polysaccharides in the marine environment and
Kolter, R. and Maloy, S. (eds.) (2012). Microbes and Evolution: The their interactions with heterotrophic bacteria. Environ. Microbiol. 20:
World That Darwin Never Saw. ASM Press. 2671–2685.
Lawton, G. (2009). Why Darwin was wrong about the tree of life. New Nissimov, J. I. and Bidle, K. D. (2017). Stress, death, and the biological
Sci. 2692: 34–39. glue of sinking matter. J. Phycol. 53: 241–244.
Martin, W. and Embley, T. M. (2004). Evolutionary biology: Early evolu Seymour, J. R. and Stocker, R. (2018). The ocean’s microscale: A
tion comes full circle. Nature 431: 134–137. microbe’s view of the sea. In Microbial Ecology of the Oceans, ed. Gasol,
Nasir, A., Kim, K. M., Da Cunha, V., and Caetano-Anollés, G. (2016). J. M. and Kirchman, D. L., pp. 289–466, Wiley Blackwell.
Arguments reinforcing the three-domain view of diversified cellular life. Verde, C., Giordano, D., Bellas, C. M., et al. (2016). Polar marine micro
Archaea 2016: 1851865. organisms and climate change. Adv. Microb. Physiol. 69: 187–215.
Schulz, H. N. and Jørgensen, B. B. (2001). Big bacteria. Annu. Rev. Verdugo, P., Alldredge, A. L., Azam, F., et al. (2004). The oceanic gel
Microbiol. 55: 105–137. phase: A bridge in the DOM-POM continuum. Mar. Chem. 92: 67–85.
Sherr, B. F., Sherr, E. B., Caron, D. A., et al. (2007). Oceanic protists. Betts, H. C., Puttick, M. N., Clark, J. W., et al. (2018). Integrated genomic
Oceanog. 20: 130–134. and fossil evidence illuminates life’s early evolution and eukaryote origin.
Suttle, C. (2005). The viriosphere: The greatest biological diversity on Nat. Ecol. Evol. 2: 1556–1562.
Earth and driver of global processes. Environ. Microbiol. 7: 481–482. Bolhuis, H., Cretoiu, M. S. and Stal, L. J. (2014). Molecular ecology of
microbial mats. FEMS Microbiol. Ecol. 90: 335–350.
30 References
Bradley, J. A., Amend, J. P., and LaRowe, D. E. (2019). Survival of the Dick, G. J., Anantharaman, K., Baker, B. J., et al. (2013). The microbiol
fewest: Microbial dormancy and maintenance in marine sediments ogy of deep-sea hydrothermal vent plumes: Ecological and biogeographic
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MARINE MICROBIOLOGY

ECOLOGY & APPLICATIONS

© 2020 by Taylor & Francis Group, LLC

No claim to original U.S. Government works

Printed on acid-free paper

International Standard Book Number-13: 978-0-367-18356-1 (Paperback)

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Genomic fingerprinting can be used to assess diversity

Microbes obtain energy from light or oxidation of

and archaeal taxonomy 48

Microbes differ in their source of carbon to make

DNA sequence data are used for identification and

DGGE and TRFLP can be used to assess composition

Elucidating the full genome sequence of microbes

provides insights into their functional roles 52

Metabarcoding and metagenomics have led to major

advances in microbial community analysis 53

Omics technologies provide information about the

functional gene composition of a microbial community 55

Genomes can now be obtained from single cells in

IN SITU ACTIVITY OF MICROBIAL COMMUNITIES 57

Many bacteria oxidize sulfur compounds 80

Microelectrodes and biosensors measure microbial

Many chemolithotrophs use hydrogen as an

processes at the microhabitat scale 57

Radioisotopes can be used to detect metabolic activity

Bacterial and archaeal nitrification is a major process

in the marine nitrogen cycle 81

Stable-isotope probing (SIP) tracks fluxes of nutrients in

Ammonia can also support anaerobic

NanoSIMS allows metabolic transfers to be measured at

Microarrays enable assessment of gene activity in the

Metatranscriptomics, metaproteomics, and metabolomics

reveal microbial activities in the environment 59

Microfluidics enables study of microscale processes 60

Mesocosm experiments attempt to simulate natural

Remote sensing permits global analysis of microbial

References and further reading 62

Chapter 3 Metabolic Diversity and

A BRIEF OVERVIEW OF CELL STRUCTURE AND

Bacteria and archaea show a variety of cell forms and

The cytoplasmic membrane controls cell processes via

transport of ions and molecules 66

Cells may contain organelles, microcompartments, and

The nature of the cell envelope has a major effect on

Genome size and organization determines bacterial and

Microbes use a variety of mechanisms to regulate

Marine bacterioplankton use two trophic strategies 92

Growth rate and turnover of organic material depend on

Copiotrophic marine bacteria may show rapid growth

Bacteria adapt to starvation by coordinated changes to

Some bacteria enter a “viable but nonculturable” state

Many bacteria use motility to search for nutrients and

Flagella also have a mechanosensory function 97

Microbes also respond to light, magnetic fields, and

other stimuli 100

Gliding and twitching motility occur on surfaces 100

Microbes colonize surfaces via formation of biofilms 101

Pili are important for bacterial attachment to surfaces

and genetic exchange 102

Antagonistic interactions between microbes occur on

particles or surfaces 102

Quorum sensing is an intercellular communication