Environmental Microbiology (2021) 23(7), 3335–3344 doi:10.1111/1462-2920.

15499

Special Issue Article

Astrobiology of life on Earth

John E. Hallsworth ,1* Rocco L. Mancinelli ,2 14

Centro de Biología Molecular Severo Ochoa,
Catharine A. Conley,3 Tiffany D. Dallas ,1 Universidad Auto noma de Madrid (CBMSO, CSICUAM),
Teresa Rinaldi ,4 Alfonso F. Davila,3 Cantoblanco, Madrid, 28049, Spain.
Kathleen C. Benison ,5 Alexander Rapoport ,6 15
Centro de Astrobiología (CAB, INTA-CSIC), Torrejon
Barbara Cavalazzi,7 Laura Selbmann ,8,9 de Ardoz, 28055, Spain.
Hitesh Changela,10,11 Frances Westall,12 16
School of Biological Sciences, Department of
Michail M. Yakimov,13 Ricardo Amils 14,15 and Microbiology, Southern Illinois University, Carbondale,
Michael T. Madigan16 IL, 62901.
1
Institute for Global Food Security, School of Biological
Sciences, Queen’s University Belfast, 19 Chlorine
Gardens, Belfast, BT9 7BL, UK. Summary
2
Bay Area Environmental Research Institute, NASA Astrobiology is mistakenly regarded by some as a
Ames Research Center, Mountain View, CA, 94035. field confined to studies of life beyond Earth. Here,
3
NASA Ames Research Center, Mountain View, CA, we consider life on Earth through an
94035. astrobiological lens. Whereas classical studies of
4
Department of Biology and Biotechnology, Sapienza microbiology historically focused on various
University of Rome, Rome, 00185, Italy. anthropocentric sub-fields (such as fermented
5 foods or commensals and pathogens of crop
Department of Geology and Geography, West Virginia
University, Morgantown, WV, 26506-6300. plants, livestock and humans), addressing key bio-
6
Laboratory of Cell Biology, Institute of Microbiology and logical questions via astrobiological approaches
Biotechnology, University of Latvia, Jelgavas Str., 1-537, can further our understanding of all life on Earth.
Riga, LV-1004, Latvia. We highlight potential implications of this
7
Department of Biological, Geological and approach through the articles in this Environmental
Environmental Sciences, University of Bologna, Microbiology special issue ‘Ecophysiology of
Bologna, 40126, Italy. Extremophiles’. They report on the microbiology of
8
Department of Ecological and Biological Sciences, places/processes including low-temperature envi-
University of Tuscia, Viterbo, 01100, Italy. ronments and chemically diverse saline- and
9 hypersaline habitats; aspects of sulphur metabo-
Italian Antarctic National Museum (MNA), Mycological
lism in hypersaline lakes, dysoxic marine waters,
Section, Genoa, 16128, Italy.
10 and thermal acidic springs; biology of extremo-
Key Laboratory of Earth and Planetary Physics,
phile viruses; the survival of terrestrial
Institute of Geology and Geophysics, Chinese Academy
extremophiles on the surface of Mars; biological
of Sciences, Beijing, 100029, China.
11
soils crusts and rock-associated microbes of
Department of Earth and Planetary Science, University
deserts; subsurface and deep biosphere, including
of New Mexico, Albuquerque, NM, 87131.
12
a salticle formed within Triassic halite; and interac-
CNRS, Ctr Biophys Mol UPR 4301, Rue Charles tions of microbes with igneous and sedimentary
Sadron, CS 80054, Orleans, F-45071, France. rocks. These studies, some of which we highlight
13
Institute of Marine Biological Resources and here, contribute to our understanding of the spa-
Biotechnology, IRBIM-CNR, Messina, 98122, Italy. tiotemporal reach of Earth’sfunctional biosphere,
and the tenacity of terrestrial life. Their findings
will help set the stage for future work focused on
Received 1 April, 2021; accepted 2 April, 2021. *For correspon-
dence. E-mail [email protected]; Tel. +442890972314; Fax the constraints for life, and how organisms adapt
+442890975877. and evolve to circumvent these constraints.

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and
reproduction in any medium, provided the original work is properly cited.
3336 J. E. Hallsworth et al.
The astrobiology of Earth iv. how do microbes determine planetary health and how
does planetary health impact the biosphere (Cavicchioli,
The field of astrobiology includes the search for life
et al., 2019);
beyond Earth. However, no traces of extraterrestrial life
v. how long can cells and communities persist through
have yet been found despite missions dedicated to its
geological time;
detection on Mars, starting with the 1976 Viking
vi. how and where did life originate;
landers (Soffen and Snyder, 1976) and extending to
vii. could life plausibly occur beyond Earth; and
the currently active Curiosity and Perseverance rovers
viii. do the laws of chemistry and physics dictate the
(Gomez-Elvira et al., 2014; Voosen, 2021). In addition,
same basic biochemistry for life everywhere it is
there have been searches for evidence of life else-
found in the universe, or even beyond?
where in the Solar System and in relation to exoplanets
but as yet have no evidence of life in these locations These are lines of enquiry that generally cannot be
either. We might therefore forgive sceptics who con- addressed via laboratory-based experiments using
sider astrobiology somewhat esoteric, or even an oxy- canonic microbes that are copiotrophic, mesophilic, aero-
moron. Here, we take the view that, in addition to the bic and heterotrophic. Instead, we need to look at the
value of the astrobiology field in relation to consider- spatiotemporal fringes of Earth’s biosphere represented
ations of life in extraterrestrial locations, astrobiological by the biology of microorganisms that are atypical and
approaches augment traditional biological studies even extreme in their nutrition (e.g. chemolithotrophs) and/or
when used with the sole purpose of understanding life their stress biology, such as halophiles, psychrophiles
on Earth. This Environmental Microbiology special and polyextremophiles. Even higher-ranked taxa that are
issue ‘Ecophysiology of Extremophiles’ explores the widely known as mesophiles (for temperature and water
value of astrobiology as a lens through which to under- activity) can have extremophilic members; for example,
stand present-day terrestrial life. Indeed, astrobiology the extremely halophilic genus Wallemia within the fungal
gives rise to novel scientific questions, technologies division Basidiomycotina (Zalar et al., 2005; Stevenson
and experimental approaches; unexplored theoretical et al., 2015). These extremophilic microbes colonize hab-
frameworks; and other insights into life on Earth that itats that are too hostile for the vast majority of life and
we otherwise would not have (Prasad et al., 2021). are among those organisms at an interface where active
With the exception of many remarkable extremophiles biology must wrestle with the thermodynamic constraints
(some of which are showcased in this special issue), his- on cellular biochemistry and structures.
torically the science of microbiology has revolved around
cultivatable microbes that are unremarkable in their
stress biology, grow well at high nutrient concentrations ‘Ecophysiology of Extremophiles’ special issue
and/or are not lithosphere-dwelling taxa. These include
human commensals and pathogens, such as Escherichia This special issue includes studies on diverse types of
coli and Salmonella species; microbes used as model extremophile systems and extreme environments. Life on
systems for studies of biochemistry (e.g. Saccharomyces Earth (and, presumably, putative life beyond our planet)
cerevisiae); microbial pathogens of crop plants or live- is usually exposed to multiple, concomitant stresses
stock; and microbes in fermented foods, such as lactic (or stressful events) such as those in polyextreme envi-
acid bacteria. Such microorganisms are, in general, of ronments (Johnson et al., 2015; Hallsworth, 2019). Martí-
the greatest concern to the daily lives of humans. nez et al. (2021) carried out a study of low water-activity
However, to address some of the most-profound ques- and osmotically stressful chaotropic brines located at
tions in biology, we often need to take on a mindset that high altitude in the Salar de Uyuni salt pan (Andes Moun-
is rooted outside Earth’s biosphere (as if we are looking tains). At the surface, microbes are also exposed to high
in); a mindset that is interdisciplinary - rather than ultraviolet radiation (primarily UV-A) and considerable
employing an approach that is anthropocentric and/or fluctuations in temperature and relative humidity. At the
more narrow. Here, we argue that this mindset is, in surface and in the subsurface, Archaea and Bacteria
essence, provided by and is best described as occur in brines or thin, briny films that consist of dis-
astrobiology. solved NaCl and the chaotropic salts MgCl2, LiCl and
Some of the (long-standing) biological questions yet to NaBr (and lower concentrations of other substances).
be properly resolved are: Environmental samples from the surface and subsurface
(to a depth of 80 m) were used to characterize spatial
i. what is life (Schrödinger, 1944; Cleland, 2019); and temporal variations in microbial communities. Intrigu-
ii. what permits and what constrains active life; ingly, the water activity of the Salar-de-Uyuni system
iii. where is life on Earth and when is it active/inactive; (0.856–0.618; Martínez et al., 2021) straddles the

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
 Astrobiology of Earth 3337
currently recognized limit for cellular activity of halophilic surpassed in terms of both biological tolerance of the cell
prokaryotes (0.635; Stevenson et al., 2015). Consistent and biophysical tolerance of some biomacromolecules.
with this finding, Martínez et al. (2021) identified taxa that Therefore, additional amounts of salt do not add to the
are known to be capable of proliferating at water activities chaotropic activity, and any values derived by extrapolat-
lower than that of saturated NaCl (whch is about 0.755). ing beyond this point are only hypothetical, as described
The Martínez et al. study provides the first insights into by Hallsworth et al. (2007) and Yakimov et al. (2015).
the microbiology of an underground chaotropic habitat Therefore, the apparent limitation of the chaotropicity-
and reveals marked differences between surface and quantification technique (Cray et al., 2013) at high molar
subsurface communities. concentrations of MgCl2 is in reality a biologically perti-
Duran-Viseras et al. (2021) used a culturomics-based nent indication that there is no further chaotropic activity.
approach (Bilen et al., 2018) to isolate novel microbial The authors of Fisher et al. (2021) were also involved in
taxa from hypersaline environments; two solar salterns in a study by Klempay et al. (2021), which analysed
southwest Spain. They identified four halophile strains Archaea and Bacteria and water chemistry, in salterns
belonging to a thus-far undiscovered haloarchaeal genus hosting a range of evaporated seawater from San Diego
that they named Halosegnis. The analyses of Dura n- Bay (southern California, USA). The Klempay et al. study
Viseras et al. (2021) revealed these to be heterotrophic has implications for interactions of chaotropicity and
aerobes containing halorhodopsin and that they repre- water activity in relation to biophysical constraints on cel-
sent two new species, for which they proposed the lular activity, an issue pertinent to diverse microbial sys-
names Halosegnis longus sp. nov. and Halosegnis tems (Hallsworth et al., 2007; Alves et al., 2015; Cray
rubeus sp. nov. By searching previously published meta- et al., 2015). Klempay et al. (2021) also used geochemi-
genomic datasets obtained from saline and hypersaline cal modelling to speculate that even brines saturated with
lakes, salterns and deep-sea brines (in North America, respect to epsomite (MgSO4) and carnallite
Europe and Asia), the authors found evidence of the (KMgCl3
6H2O) can potentially be inhabited by active hal-
genus Halosegnis in geographical locations worldwide. In ophiles; that is, at less than 0.600 water activity which
habitats with intermediate salinities (from 18% to 27%, is a value consistent with empirical data for cell division
wt./vol.), these Archaea reached the highest abundance, of halophilic/xerophilic Aspergillus penicillioides at high
up to 8% of the prokaryotic communities. Metagenomics glycerol concentration (Stevenson et al., 2017). The work
and other culture-independent techniques used in studies of Klempay et al. makes a strong case that the search for
of environmental microbiology have revealed a vast gap life on Mars should focus on past saline environments.
between the number of microorganisms we are able to Although any putative life in our Solar System beyond
cultivate and the numbers of taxa actually present in situ; Earth is likely to be anaerobic (as was early life on Earth),
the latter are orders of magnitude greater than the former we cannot know whether terrestrial-type life on
(Whitman et al., 1998; Lloyd et al., 2018). However, exoplanets - or, in a multiverse scenario, beyond our uni-
culture-independent techniques can also be prone to verse (Adams and Grohs, 2017) - would necessarily be
errors, including those caused by contamination; incom- anaerobic. This would depend on the longer-term condi-
plete gene databases or faulty data inputs within such tions of habitability on extraterrestrial rocky planets
databases; lack of insight into metabolic activity, pheno- (Westall et al., 2015; Gebauer et al., 2018). That said,
type, or physiological and phenotypic plasticity/capability; terrestrial anaerobes are highly pertinent to astrobiology
and ecological interactions. Dura n-Viseras et al. (2021) research (Westall et al., 2015; Beblo-Vranesevic
used diverse culture conditions (either rich organic or oli- et al., 2020). In the current special issue, Sorokin
gotrophic medium) and new protocols to combine meta- et al. (2021) conceptually defined an independent and
genomics with culturing techniques, demonstrating that self-sufficient hypersaline anoxic ecosystem based solely
culture-based approaches are crucial for understanding on sulphur-respiring haloarchaea. The authors isolated
the evolutionary, metabolic and ecological importance of neutrophilic haloarchaea from hypersaline salt lakes, and
individual species. We anticipate that similar studies will a natronoarchaeon from soda lakes, of Russia. These
become increasingly important in the near future, for vari- halophiles represent analogues of ‘primary’ anaerobes, a
ous microbial systems. functional subgroup of sulphur-respiring haloarchaea that
In a comprehensive review of athalassohaline deep- was thus-far unknown in culture. The neutrophilic
sea hypersaline anoxic brines, Fisher et al. (2021) point haloarchaea are carbohydrate-fermenting, and produce
out that the art of extrapolating chaotropicity values can H2 in the absence of electron acceptors but switch to res-
be imprecise. We agree with this finding and believe that piration in the presence of sulphur, thiosulphate, or
this is because, beyond specific concentrations of highly dimethylsulphoxide (DMSO). The non-fermentative, sac-
chaotropic salts, the chaotropicity limit has been charolytic natronoarchaeon is able to grow anaerobically

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
3338 J. E. Hallsworth et al.
only in the presence of sulphur compounds as electron fluids that move through fractures in crustal rocks. The
acceptors. The discovery of the metabolic capabilities of deep biosphere is actively involved in global nutrient
these microorganisms demonstrates that a self-sufficient cycles, pollutant degradation, and the formation and
community consisting of three subgroups of sulphur- weathering of rocks. Orcutt et al. (2021) report a study
respiring haloarchaea could completely mineralize carried within the oxic oceanic crust on a flank of the
organic carbon in anoxic sediments, starting from Mid-Atlantic Ridge. Minerals were inserted into bore-
carbohydrates. holes and microbial colonization was assessed over
A minireview by van Vliet et al. (2021) explores time. These minerals were ‘igneous silicates (basalts,
microbe-mediated sulphur cycling in dysoxic marine fayalite, olivine), metal sulphides (pyrite, pyrrhotite,
waters where oxygen levels fall below the usual limits of sphalerite, chalcopyrite), metal oxides (haematite, goe-
detection (<1 μM). Over the past 60 years, dysoxic thite), metal carbonate (siderite) and less-reactive sur-
marine waters - a hotspot for anoxic metabolic cycling - faces including glass beads, glass wool and plastic’
increased more than fourfold (by volume) due to global (Orcutt et al., 2021). Remarkably, microbial growth
warming. A network of phylogenetically and (determined by factors such as water/rock ratios, fluid
ecophysiologically diverse microorganisms mediates temperature and oxygenicity) did not correlate with
redox reactions between sulphate (SO42−) and hydro- mineral type. One of the most-abundant microbial taxa
gen sulphide (HS−), including their sulphur-bearing present was the bacterial family Rhodobacteraceae
intermediates. The biochemical sulphur cycle is an (Orcutt et al., 2021). During the study period (several
important component of the global biogeochemical years), biodiversity of biofilm-forming microbes that col-
cycling of Earth’s oceans. Knowledge of sulphur onized the mineral surfaces increased. One of the taxa
cycling is also pertinent to models designed to evaluate that became more abundant was Thioprofundum,
the biological potential of aquatic environments beyond which the authors speculate could be used as an indi-
Earth. One example is ancient lakes on Mars, whose cator of the stage of colonization. The presence of all
remnant sediments are currently being explored by these microbes is evidence that there has been an inti-
NASA’s Curiosity and Perseverance rovers (sulphur- mate interrelationship between microbes and volcanic
bearing minerals and organics have already been dis- substrates that dates back to the earliest terrestrial life
covered by Curiosity, providing tantalizing hints of a forms more than 3.5 billion years ago (Westall
possible sulphur cycle on ancient Mars). Other, more et al., 2015). It is biofilm-forming microbes
distant examples are the dark oceans that lie beneath (i.e. Archaea and Bacteria similar to those in the Orcutt
some icy moons in the outer Solar System, such as et al. study) that dominated the rocky habitats of the
Saturn’s moon Enceladus, where sulphur-bearing com- young Earth prior to the appearance of photosynthesis,
pounds are known to be present. The complex web of especially oxygenic photosynthesis. The longevity of
sulphur-cycling reactions in Earth’s oceans, which has the oligotrophic, low-biomass habitat provided by the
been carefully disentangled by van Vliet et al. (2021), crust, along with the tenacity of microbial systems, has
appears to depend ultimately on a supply of oxidized permitted the persistence of life over several billions of
compounds. Although oxidative power is thought to be years.
a limiting commodity in the subsurface oceans of icy A different kind of subsurface habitat was studied by
moons, new discoveries are already revealing new or Cirigliano et al. (2021); Iron-Age tombs hewn out of a cal-
unexpected sources of oxidative power, such as the carenite and a sandstone rock. The study focused on the
potential oxidation and reduction of pyrite, a mineral microbiology of moonmilk (a layer of precipitated CaCO3
often associated with hydrothermal chimneys thought in the form of nanofibers) on the walls of these ‘anthropo-
to exist on the seafloor of Europa (Altair et al., 2018). genic caves’ that are located in central Italy at depths of
In addition, recent geochemical models point to new or 1–10 m below ground level. They are home to an
unexpected sources of oxidants in the ocean of ecophysiologically and phylogenetically diverse micro-
Enceladus (Ray et al., 2021), thereby propelling Earth- biome that the authors described as ‘primarily bacteria
based models of biochemical sulphur-cycling to the mesophilic for temperature and xerotolerance (including
forefront of ‘extraterrestrial’ astrobiology research. Actinobacteria, Bacteroidetes and Proteobacteria);…pho-
Recent studies of the Earth’s deep biosphere have tosynthetic Cyanobacteria exhibiting heterotrophic nutri-
revealed biodiverse communities in both deep-ocean tion (Calothrix and Chroococcidiopsis);…[and taxa
sediments and the Earth’s crust (e.g. Lloyd et al., 2018; known to be] psychrotolerant (Polaromonas),
Daly et al., 2019 and, in the current issue, Karnachuk acidotolerant or acidophilic (members of the
et al., 2021; Orcutt et al., 2021). Indeed, some of the Acidobacteria), or resist to ionizing radiation
most-remote environments on Earth host microbial (Brevundimonas and Truepera)’ (Cirigliano et al., 2021).
communities fed by carbon and nutrients present in the The authors determined the kinetics of moonmilk

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
 Astrobiology of Earth 3339

formation (occuring over one to several decades)⁣ and would have found refuge within the rock’s gas spaces
discussed the paradox that this underground ecosystem, during the cooling and drying of the planet.
that lacks primary production, is apparently highly active. Pavankumar et al. (2021) analyse the molecular biol-
Other special issue articles also focus on interactions ogy of the cold-active bacterium Pseudomonas syringae
of microbes with minerals and igneous or sedimentary that is a model for unravelling the effects of low tempera-
rocks (Kang et al., 2021; Wu et al., 2021). There is inter- ture on the molecular infrastructure of cells and uses the
est in biomining of rare earth elements beyond Earth full suite of biochemical and genetic tools now available.
(McLeod and Krekeler, 2017), and bacteria have been Their review focuses on the effects of cold on
proposed previously for this purpose (Cockell membrane-mediated and enzymatic activities, in particu-
et al., 2020). In the current special issue, Kang lar enzymes that catalyse replication and transcriptional
et al. (2021) now examine the influence of Aspergillus events. One insightful concept, considered for the first
niger on the weathering of monazite, a phosphate- time, is how changes in the density of water that occur
mineral source of rare earth elements such as Ce, La around 4 C appear to impact the biology of the cell. Not
and Nd. Culture-based studies that involved addition of only membranes but also cytoplasmic viscosity, protein
monazite to the growth medium were used to unravel the structure and enzymatic catalysis can be affected by den-
biophysical/biogeochemical process of rock degradation sity changes in the biophilic solvent, water. Given that
by this ascomycete, including the production of organic temperature is one of the most significant environmental
acids such as citric acid and oxalic acid. Kang controls on microbial growth, this review brings the
et al. (2021) provides fundamental knowledge on the reader up to speed on cold-related molecular barriers to
microbial processing and potential utilization of these life and known mechanisms for overcoming them.
important elements on Earth and potentially on other Several Bacteria are capable of subzero growth, and
planetary bodies in the future. microbial communities may exist in some of Earth’s col-
A number of the special issue articles focus on life at dest environments, such as the interior of Antarctica
low temperatures in the Arctic or Antarctic (Coleine (Madigan et al. 2017; Hayward et al. 2021). This indi-
et al. 2021; Mudge et al., 2021; Pavankumar et al., 2021; cates that extreme cold is not an insurmountable barrier
Magnuson et al., 2021). These habitats are typically poly- for terrestrial (and presumably extraterrestrial) life. The
extreme due to combinations of extreme cold, low water- special issue article by Mudge et al. (2021) probes physi-
activity, long-term desiccation and freezing, salt(s), ultra- ological features of Colwellia psychrerythraea, a
violet radiation, low-nutrient conditions, and/or events that polyextremophilic bacterium isolated from subzero
can be traumatic for the cell such as desiccation– marine sediments that can grow at a salinity up to 18%
rehydration (in some cases, caused by salt (wt./vol.) and at temperatures as low as −12 C. As such,
deliquescence–efflorescence) and freeze–thaw cycles and because its genome and many unusual biochemical
(Hallsworth, 2018). To date, studies of cryptoendolithic features are already known, C. psychrerythraea has risen
communities of the Antarctic were concentrated on the to become a model marine psychrophile for the study of
McMurdo Dry Valleys and the Transantarctic Mountains carbon cycling in cold marine sediments, and a relevant
of Victoria Land. Coleine et al. (2021) report on crypto- subject for assessing growth and survivability under sim-
endolithic microbes in sedimentary rock (sandstone) in a ulated Martian conditions. Using radiotracer methods,
newly explored area (Helliwell Hills, North Victoria Land). previous studies of this bacterium revealed protein syn-
The authors conducted a comparative study of biodiver- thesis in unamended cell suspensions at −20 C and in
sity data from these rocks and data from previous studies those supplemented with additional extracellular poly-
of sandstones located at more than 30 other sites in Vic- meric substances at −80 C. Mudge et al. (2021) now uti-
toria Land. This revealed that both alpha- and beta- lize proteomic tools to reveal metabolic pathway-specific
diversity were strongly correlated to geography and that proteins produced by C. psychrerythraea in response to
the most-remote region of Helliwell Hills hosts an uncom- variations in temperature, salinity and nutrient status. In
mon type of microbial community including Archaea and addition, useful new tools emerge from their research
lichen such as Lecidella grenii (Coleine et al., 2021). including a novel approach for life detection that identifies
Such investigations, on pristine Antarctic environments, over 500 very short peptides whose sequences could be
can provide insights into the ecology and evolution of determined by either lander-based or in-orbit mass spec-
early life on Earth and can inform investigations into the trometers and used as potential biosignatures of cold- or
habitability of extraterrestrial environments (Cockell hypersaline metabolisms.
et al., 2016). Sandstones and other rocky substrates on Also on the topic of life at subzero temperatures, Mag-
early Mars may have supported putative Martian life nuson et al. (2021) present a comprehensive, multi-
(Wierzchos et al., 2012), since cryptoendolithic life forms phase study of a microbial community thriving in a

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
3340 J. E. Hallsworth et al.
perennial system of (hypersaline, low-temperature) An environment that is widely used as an analogue for
springs located in the Canadian High Arctic. This unusual the Mars’ surface is the Atacama region in Chile (Aerts
ecosystem is underlain by permafrost, with water temper- et al., 2020; Nagy et al., 2020). In the current special
atures consistently close to zero, and is anoxic, oligotro- issue, Uritskiy et al. (2021) give a comprehensive over-
phic and rich in reduced sulphur compounds. These view of an extremophile community on halite nodules at
waters are dominated by a sulphide-oxidizing the surface of the Atacama Desert. The NaCl-saturated
chemolithoautotrophic bacterium of the genus brine films here are exposed to intense ultraviolet radia-
Thiomicrorhabdus which is present within streamers tion and prone to cycles of salt efflorescence–
(made up of microbial biomass), while Actinobacteria, deliquescence (Hallsworth, 2020). Combining meta-
Bacteroidetes and Cyanobacteria make up the rest of the genomic and metatranscriptomic analyses (in both light
community. Multiphasic-omic tools, supported by an iso- and dark conditions), Uritskiy et al. (2021) identify
topic approach, have deciphered the contribution of this microbes responsible for the essential metabolic func-
(apparently new) species of Thiomicrorhabdus to sulphur tions. One important finding was that the only eukaryote
cycling and primary production. It is very likely that this of the community, a novel Dolichomastix alga, is the
CO2-fixing organism is responsible for the functioning of major contributor of photosynthetic transcripts. An addi-
the entire streamer ecosystem. The microbial community tional key finding was that new halophile viruses exhibit
and biogeochemistry of the Magnuson et al. springs are transcriptional activity, indicating an active role in
qualitatively different from those of spring systems infecting their hosts in the halite-associated brines of this
located in other cold regions (Roy et al., 2020; Knuth and dry desert region (mainly Halobacteria and Salinibacter).
Potter-McIntyre, 2021). The light-independent Another study that raises intriguing questions about Mars
chemolithoautotrophic microbial community flourishing in is that of Thompson et al. (2021), which focuses on the
the High Arctic (Magnuson et al., 2021) has implications microbiology of a subsurface NaCl stalactite within a Tri-
for the possibility of life existing in cold places beyond assic halite deposit. The study reveals the microbiome of
Earth. this structure, located in Northern Ireland (North West
Also relating to a cold location, an research paper by Europe). It also reveals ecophysiological functions of the
Hallsworth (2021) examines whether the surface/near- resident microbes, and describes the habitat as one of
surface of Mars is biocidal to all life. He gives an over- stable in temperature (17 C) and water activity (0.755),
view of the suite of Mars surface conditions that are often and consistent water supply. The authors convincingly
considered incompatible with the survival of terrestrial argue that saline speleothems (structures formed of pre-
extremophiles. This article coaxes the reader to consider cipitated salt) located in the Mars subsurface could
a putative (Mars-based) terrestrial microbe from a Mars- potentially hostancient Martian life at depths where tem-
centric point of view. The Earth, that appears in general peratures permit.
to be hospitable for humans, is highly oxidative so may A special issue study of a different kind of extreme
be a challenging place for putative microbial life that has (aqueous) environment used comparative genomics to
evolved elsewhere. Oxygen is extremely toxic to strict study Archaea of the order Sulfolobales and identified
anaerobic microbes and requires special adaptations to characteristics that enable life, in thermal acid springs
evolve over a long timescale to be tolerated, detoxified (Counts et al., 2021). Evidence is presented by the
and utilized (indeed, life could never have emerged in an authors that, collectively, these microbes have diverse
oxidized environment). A major environmental change on oxygen-consuming protein complexes; are able to detox-
Earth was caused by the evolution of oxygenic photosyn- ify sulphur and utilize it lithotrophically (for energy gener-
thesis in Cyanobacteria about 3 billion years ago ation); and are capable of pH homeostasis under highly
(Blankenship and Hartman, 1998). Anaerobic life forms acidic conditions. Their metabolic versatility in these
that were unable to evolve mechanisms to deal with ways is consistent with their thermo- and acidophilic phe-
slowly rising oxygen levels likely either died off or ret- notype and their ability to colonize geothermal habitats
reated to the anoxic niches where they remain today. For that can be abundant in H2S and S0. Given the recent
other microbes, an oxygenated planet provided an oppor- interest in the question of habitability in the sulphuric acid
tunity for life to diversify through the evolution of powerful clouds of Venus, the acid-, temperature- and
energy-conservation mechanisms based on aerobic res- xerotolerance of terrestrial polyextremophiles has
piration. The analysis elaborated by Hallsworth (2021) become a resurgent topic (Greaves et al., 2021;
indicates that Mars’ surface may not be lethal to all kinds Hallsworth et al., 2021).
of terrestrial microbes; this emphasises the necessity of Two papers in this special issue describe the structure
planetary protection measures during exploration of genomes in taxonomic orders within the
missions. Euryarchaeota and reflect on how genome structure may

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
 Astrobiology of Earth 3341
contribute to the success of archaeal lineages. Zhong organisms, and thereby gain functions that improve their
et al. (2021) retrieved whole-genome sequences for survival or invasiveness on Earth?
30 species within the order Thermococcales from the
public sequence databases. A core group of functional
genes were found to be present in all 30 species, as well Concluding remarks
as ‘accessory’ and ‘unique’ genes present in only some Both the current article and the other articles in this spe-
member species of the order that serve diverse functions cial issue focus mainly on studying life on Earth but,
relating to habitat and lifestyle, among them importantly, include approaches from astrobiology. In
extremotolerance. Zhong et al. suggest that common some cases, they also discuss issues pertaining to life
adaptation mechanisms within the Thermococcales hint beyond Earth. Although astrobiology has always included
at survival strategies for extreme conditions likely to have studies of terrestrial life (whether past, present or future),
been present on the early Earth and possibly also pre- the latter have not always included the former. Indeed,
sent in extraterrestrial environments. the etymology of the term astro- (star or celestial) -biol-
Hu et al. (2021) performed whole-genome environmental ogy (the story/study of life) is somewhat misleading. Nev-
sequencing on samples retrieved from a black-odorous river ertheless, we believe that astrobiology utilizes its own set
in China, a habitat containing pollutants that can cause cel- of approaches and that studying Earth’s biology from an
lular stress/toxicity by various mechanisms (e.g. Bhaganna astrobiology-inspired perspective can give rise to novel
et al., 2010). Sequencing was carried out after dis- scientific questions and scientific findings. For example,
aggregating the samples into slurry and allowing the sedi- the Coleine et al. (2021) paper focused on sandstone in
mentary structure to re-form in the laboratory. This Antarctica a Mars analogue site to reveal aspects of the
approach represents a successful compromise between terrestrial endolithic ecosystem. Another study, of bio-
sequencing environmental samples immediately after col- physical limits for biotic activity of terrestrial
lection, when organisms of interest may be rare, and the extremophiles that focused on the question of habitability
laboratory culture in which an ecological community is dis- of Venus’ atmosphere, discovered that the ecophysiologi-
aggregated into the component members and only those cal constraints of the ultimate acidophile are apparently
able to grow in isolation are studied. From the environmen- determined by xerotolerance (Hallsworth et al., 2021).
tal sequences obtained, Hu et al. assembled nearly com- Modern science has become more specialist (and more
plete genomes for four new species within the taxonomic reductionist) as scientific fields fragment into distinct sub-
class Thermoplasmatales, members of which are known for fields. This trend does not favour syncretistic approaches
acid tolerance. They identified a further five partial genomes that integrate disparate lines of evidence (Ehrenzweig,
assembled from environmental sequences available in pub- 1970)); approaches that might help to address key ques-
lic sequence databases and propose that these genomes tions in biology. We believe that the interdisciplinary and
are sufficiently divergent to represent a new candidate cross-cutting field of astrobiology can enhance our under-
order, Candidatus Gimiplasmatales. Within these genomes, standing of terrestrial life by acting counter to an exces-
Hu et al. identify consistent groups of genes that could be sively narrow focus. In addition, new and miniaturized
capable of metabolizing complex organic compounds as technologies have been created by the field of astrobiol-
well as de-novo synthesis of nucleic acids and mevalonate. ogy, and these can have important applications for study-
Zhong et al. (2021) report the expansion of accessory ing life on Earth. These include miniaturised bioreactors,
genes in the genomes of Thermococcales, and Hu sequencers, spectrophotometers (Castro-Wallace et al.,
et al. (2021) provide evidence that one mechanism for 2017; Massaro Tieze et al., 2021); sterilisation methodolo-
such expansion is lateral gene transfer. The genomes of gies (Craven et al., 2021); a water-activity sensor (Desai
Candidatus Gimiplasmatales include genes for arsenic et al., 2021); and protocols for life detection (Kminek
detoxification and cell motility. A set of genes involved in et al., 2014; Abrahamsson et al., 2021). The articles pres-
the Wood–Ljungdahl carbon-fixation pathway appears to ented in this special issue also contribute to our under-
have been obtained from the Firmicutes. This evidence standing of the nature and tenacity of life on Earth. They
for gene transfer between Archaea and Bacteria, two dif- also help set the stage for future exploration of the various
ferent domains of Earth life, raises important questions constraints on terrestrial life and how organisms strive to
around planetary protection and appropriate precautions circumvent these constraints.
to take when studying extraterrestrial life should we find
it. For instance, could Earth organisms take up DNA from
extraterrestrial organisms (assuming that the latter also Acknowledgements
use DNA as genetic material) and gain novel, potentially Funding was provided by the Biotechnology and Biological
hazardous functions. Alternatively, could extraterrestrial Sciences Research Council (BBSRC, United Kingdom) pro-
organisms that use DNA take up genes from Earth ject BBF003471.

© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.,
Environmental Microbiology, 23, 3335–3344
3342 J. E. Hallsworth et al.
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