Renewable and Sustainable Energy Reviews 65 (2016) 832–840

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews

journal homepage: www.elsevier.com/locate/rser

Energy by Microbial Fuel Cells: Scientometric global synthesis and challenges

art ic l e i nf o a b s t r a c t

Keywords: The scarcity of natural resources and the growing need for electricity requires the development of new
Scientometry technologies that can provide alternatives to traditional energy sources in a sustainable fashion. One of
Biotechnology the promising opportunities currently under development is Microbial Fuel Cell (MFC) technology. The
Bacteria aim of our study was to analyze the relevant literature related to MFCs through a scientometric approach
Sustainable power generation in order to produce a comprehensive synthesis, something that is lacking. We identified 19671 relevant
Electricity production studies in the field and examined 3427 papers in detail in a systematic review performed in the ISI
Biodiversity database Web of Science. Our primary goals were to: (i) determine the temporal evolution of publica-
tions, (ii) reveal which journals publish on the subject, (iii) show the global distribution of MFC research
and funding perspectives, (iv) uncover the scales of application of the technology, (v) account for the
most commonly used substrates, (vi) find out whether pure or mixed cultures of microorganisms are
involved and (vii) determine the major species used. We detected a substantial increase in publications
after 2006. We found that the US and East Asia are the most promising locations for the development of
MFCs, given both the number of publications and the amount of financial investment in research and
development. The main technological barrier to the wide-spread use of MFCs is the scale of application,
restricted to small prototypes insufficient to generate electricity for practical purposes. The most cited
substrate was wastewater, both domestic and industrial, demonstrating the great potential of MFCs in
wastewater treatment. Finally, our results demonstrated that there is a wide variety of microorganisms
capable of generating electricity, although the great majority of papers focus on a few well-established
species. Taken together, our results can help research and application in this field on a global level
perspective.
& 2016 Elsevier Ltd. All rights reserved.

1. Introduction between chambers. The protons generated by the process of oxi-

dation migrate from the anaerobic (anode) to the aerobic (cathode)
The global demand for energy has grown considerably in recent compartment through the membrane, while the generated electrons
decades [1]. The massive growth of the human population [2] is move to the cathode through an external circuit. A wide variety of
associated with huge increases in energy consumption, resulting bacteria are able to both oxidize organic components and provide
largely from the energy available from fossil fuels and also from electrons for the fuel cell, and MFCs have been designed using either
the energy used to obtain those fuels [3]. Moreover, the traditional pure or mixed cultures of bacteria [11]. The choice of microbial
sources of energy, such as fossil fuels, are becoming scarce [4]. species and the subsequent efficiency of the MFCs depend on the
Because of this upcoming energy crisis, there is a need for tech- cell configuration and on characteristics such as substrate compo-
nological innovation [3] or renovation of the current patterns of sition and concentration [10,12]. MFCs could be adaptable to a sus-
energy use by humanity. It is, therefore, mandatory that we find tainable pattern for wastewater treatment and production of do-
innovative energy sources that are environmentally less damaging mestic energy [13], so they are a promising sustainable technology
and can be used in a sustainable fashion [5]. Several alternative with huge advantages over other technologies, including lower en-
sources of clean and renewable energy, which currently represent ergy consumption, small environmental footprint, and operational
around 20% of total world energy demand, are under development stability. However, there are some drawbacks in the practical feasi-
and have enormous potential [6]. bility of MFCs, especially with respect to costs, large-scale system
The production of electricity using Microbial Fuel Cells (MFCs) is development, and energy recovery [14]. In previous reviews [i.e.
a renewable and sustainable technology that is becoming more ef- 10,15–20] of the topic there has not been an unbiased and replicable
ficient [7,8]. MFCs are devices that produce electricity using the scientometric synthesis of MFC research with the goal of assessing
metabolic energy of bacteria, the catalysts that oxidize organic and its advances and its gaps. In this sense a systematic review of the
inorganic matter [9]. Typical designs or modes of operation for MFCs subject is lacking. Systematic reviews specify search criteria on a
consist of two or one chamber components [10]. In a two-chamber particular issue and use predefined protocols, aiming at reducing
set up, an anaerobic anode chamber and an aerobic cathode bias, allowing rigorous replication, and diagnosing gaps [21]. Sys-
chamber separated by a membrane are connected through an ex- tematic reviews provide high-quality results, identifying, appraising,
ternal circuit. The membrane does not allow the exchange of oxygen and synthesizing all relevant studies on a particular topic [21,22].

http://dx.doi.org/10.1016/j.rser.2016.06.050
1364-0321/& 2016 Elsevier Ltd. All rights reserved.
 E.G. Ferreira Mercuri et al. / Renewable and Sustainable Energy Reviews 65 (2016) 832–840 833

The major aim of our study was to use a systematic review to resulting from our survey for the journal. We used y ¼8 years,
identify, appraise and synthesize the empirical evidence concerning from 2008 to 2015.
MFCs in order to answer some questions about the use of MFCs to c) Country: We considered the article's country of origin to cor-
generate electricity, highlighting tendencies and major gaps in our respond with the university address of the lead/first author,
knowledge of the topic. Our specific aims were to (i) determine the obtained through the WoS field “reprint address”. The number
temporal evolution of publications, (ii) reveal which journals publish of publications by country was related to the country's in-
on the subject, (iii) show the global distribution of MFC research and vestment in Research and Development (R&D) in terms of the
funding perspectives, (iv) uncover the scales of application of the percentage of invested Gross Domestic Product (GDP) nor-
technology, (v) account for the most commonly used substrates, (vi) malized by the Purchasing Power Parity (PPP). The gross ex-
find out whether they are based on pure or mixed cultures of mi- penditures on R&D were obtained from the 2014 Battelle re-
croorganisms and (vii) determine which are the species used. Our port “2014 Global R&D Funding Forecast”, which is based on
research used explicit methods designed to minimize bias in the data from the World Bank, International Monetary Fund, and
discovery of the trends and major gaps in MFC research. This ap- CIA Fact Book [24].
proach allows us to identify the strengths and weaknesses of this d) Technology range of application: We classified the eletro-bio-
new technology in a way that produces results that can be trusted chemical devices studied into three broad categories:
and that will help to support new research and application in this (1) bench scale, for laboratory small MFCs; (2) large scale, for
field in a global level perspective. studies carried out in large MFC plants; and (3) other appli-
cations (pilot projects), for studies involving electricity gen-
eration with microorganisms through other technologies (e.g.
2. Methodology solar microbial cells).
e) Type of substrate: The substrates used in the aqueous solution
Web of Science database publications were collected covering a of the MFCs were classified according to their chemical com-
period of 31 years from 1985 to 2015. The survey was based on the position. We classified them as natural (consisting, for most
simultaneous use of three WoS search fields, each referring to a part, of organic compounds) or synthetic (artificial/inorganic
compounds).
relevant sub-theme to build the central theme. We used Boolean
f) Pure or mixed cultures or comparative studies: We determined
operators, quotation marks, wildcards and query sets to create our
whether (1) the studies used a single microorganism to gen-
query. The sub-themes were: 1) generation of energy by micro-
erate electricity, (2) the studies used a association of micro-
organisms, search field code: fuel$ OR biofuel$ OR bioenergy OR
organisms (mixed) or (3) the studies compared the generation
“energy generat*”; 2) technology associated, search field code: cell*
and/or efficiency between pure or mixed cultures in MFCs.
OR biofilm$ OR batter* OR electr*; 3) microorganisms of interest,
g) Microorganism(s) under study: For each bacterium, we sear-
with search combination: microbial OR microbe$ OR biological OR
ched the specific taxonomic classification, the Gram stain and
bacteria* OR fung* OR algae; Because of the large number of ar-
the degree of pathogenicity to man. For non-transgenic mi-
ticles initially found, 19,671 records, the query was restricted to
croorganisms we used the MicrobeWiki database [25] (Kenyon
the title of the publication. We then refined the survey by research
College, Ohio, United States), for genetically modified micro-
area to the areas “microbiology” and “marine freshwater biology”.
organisms we used LPSN database: “List Of Prokaryotic Names
We focused on the areas of microbiology and marine freshwater
With Standing In Nomenclature” [26] (British Society for
biology since these research fields cover the great majority of
General Microbiology). The quoted frequency for each organ-
microorganisms used in MFCs and, therefore, provide a good sub-
ism was compared to the frequency of appearance in previous
sampling. The remaining articles were evaluated by their re-
reviews [10,15–20].
levance to the topic of interest by reading the titles and abstracts.
To guarantee that we maintained our focus on the aims proposed
We conducted the Pearson correlation test and graphical ana-
above we excluded publications whose contents were not related
lysis to show tendencies and relationships, and to examine the
to our aims, for example, articles dealing with specific electro-
relationship between the number of publications screened and the
chemical processes or the material composition of the electrodes. number of MFC publications in WoS. The same tests were also
After completing the initial screening, the remaining articles used to investigate the relation between the number of publica-
were analyzed by abstract, keywords, and by reading the full ar- tions and the amount of R&D investment in US$ and between the
ticle. The following information was extracted from each article: number of publications and the percentage of GDP invested in
R&D.
a) Year: The data are provided in the column “year of publication”
in WoS.
b) Journal: We determined the distribution of articles by journal, 3. Results
with the results weighted by dividing the number of relevant
publications by the number of issues of the journal published The initial search resulted in 19,671 articles, from which 3427
each year. To identify which journals published more papers passed the first screening in the ISI Web of Science database
on MFCs regardless of the total number of papers published by (Fig. 1). Of these, only 116 were actually directly related to mi-
each journal, which is very heterogeneous, we calculated a crobiology and marine freshwater biology. A total of 98 (0.5%)
relative weight w [23]: articles met the inclusion criteria during the third and final
⎛ n ⎞ screening, they are all listed in Appendix.
w =⎜ ⎟ 1000 All studies matching our criteria were published after 1999, and
⎝ pey ⎠ (1)
we detected a substantial increase in the number of publications
where p is the mean number of papers published in the first after 2007 (Fig. 2). 84.7% of the studies were concentrated in the
issue of each year , e is the number of issues per year, y is the nine-year period from 2006 to 2014. In addition, a positive cor-
number of years of analysis, and n is the number of papers relation was found between the number of publications screened
834 E.G. Ferreira Mercuri et al. / Renewable and Sustainable Energy Reviews 65 (2016) 832–840

“Microbial Biotechnology (MBT)”, 6.49 for the “Journal of Micro-

biology and Biotechnology”, and 6.08 for the “Microbes and En-
vironments” (Fig. 3). The 34 remaining journals had w o6.0. The
mean 7tandard deviation of the Impact Factor (IF) was
2.397 1.85. The journal with the highest IF was “Trends in Mi-
crobiology” (IF¼ 8.109, n¼1), followed by “Nature (The ISME
Journal)” (IF ¼7.629, n ¼6) and “Environmental Microbiology”
(IF¼ 5.657, n ¼1). There was no relationship between IF and re-
lative frequency of studies per journal.
The journal AEM had the greatest percentage of publications in
our survey, but also has a large number of editions per year (12
editions) and low relative weight (w¼2.02). JMB had also a large
number of articles published and a higher relative weight
(w¼ 6.5). The journal MBT reached the highest relative weight
(w¼ 8.2) with 6 editions per year and 4 published studies found in
our query.
Of the 25 countries with MFC publications, 52.04% of the stu-
dies were conducted in Asia, 23.47% in America, 20.41% in Europe,
3.06% in Oceania and 1.02% in Africa. Four countries (US, South
Korea, China and Japan) held the majority (62.24%) of the studies;
they also accounted for more than 1 trillion US$ of investment. The
Fig. 1. Flow chart detailing the process of record collection and study elimination Pearson correlation test showed a positive relationship between
for the field synopsis and systematic review. the number of publications and the amount of R&D investment
(r¼ 0.88, p o0.0001), but a low correlation between the number of
and the number of MFC publications in WoS (r ¼0.81, p o0.0001) publications and the percentage of GDP invested in R&D (r¼ 0.32,
for the entire period (1999–2015). In two years, 2002 and 2005, we p¼ 0.11). The number of publications by country varies from 1 (11
found zero articles and in the year of 2015 we only considered countries) to 22 (EUA) between 1999 and 2015. Fig. 4 shows the
articles published until the month of September. global distribution of the articles of the survey, the percentage of
There is a high correlation between the total number of in- GDP invested in R&D and total investment in billion dollars in
dexed publications in WoS and the number of articles about MFCs some of the countries.
(black line Fig. 2) in WoS (r ¼0.94, p o0.0001). This result clearly The analysis of the range of application of the MFCs shows that
indicates the growing potential of MFCs as a field of research. The 68% of the studies were performed on a laboratory scale and 22%
temporal trends in our sample are consistent with trends MFC in large plants. Ten percent of the papers employed generation of
research as a whole. electricity with microorganisms through technologies other than
The selected articles were published in 37 journals. Nearly half MFCs (such as microbial solar panels). Fig. 5 depicts the bar chart
of the articles (44.9%) were published in just four journals: 16.3% with the number of the articles in each scale of application.
in “Applied and Environmental Microbiology (AEM)”, 13.3% in the Approximately 60% of the studies used synthetic substrates in
“Journal of Microbiology and Biotechnology (JMB)”, 9.2% in “Inter- the aqueous solution of the MFC (Fig. 6). Glucose and acetate were
national Journal of Systematic and Evolutionary Microbiology” and the most commonly used, each of them cited in 15 articles, and
6.1% in “Nature (The ISME Journal)” (Fig. 3). The other 33 journals together account for 44% of the synthetic substrates. Industrial
published the remaining 55.1% of the studies, with seven journals waste water was used in 20% and ethanol in 7% of the studies.
(21.4%) publishing only one relevant publication over the period of Moreover, the variety of synthetic substrates is remarkable, in-
the study. The highest relative weights (w) were 8.23 for the cluding Glutamate, Azo Dye, Propionate and Fumarate, each of

Fig. 2. Temporal evolution of the number of articles related to MFCs and WoS database in the period 1999–2015. The left y-axis represents the number of publications per
year in the bar chart. The right y-axis indicates the number of papers shown in the black line, which represents the evolution of total number of articles about MFCs in WoS.
The dashed line represents the evolution all records of Web of Science (not in scale).
 E.G. Ferreira Mercuri et al. / Renewable and Sustainable Energy Reviews 65 (2016) 832–840 835

Fig. 3. Distribution of articles by journals and the relative weight w, calculated from Eq. (1). The graph shows journals with more than two publications found in our research
between 1999 and 2015.

Fig. 4. Global distribution patterns of the articles reviewed here. The color scale indicates the number of articles published by each country. The doughnut chart indicates the
percentage of Gross Domestic Product (GDP) invested in Research and Development (R&D), and Gross Expenditures on R&D (GERD) normalized by the Purchasing Power
Parity (PPP) in billions of dollars.

which was mentioned at least once. Natural substrates were

mentioned in 42 articles, approximately 40% of the studies in our
sample. The sources of the natural substrates also showed a high
diversity. Gross domestic wastewater was the most frequently
used (38%), followed by lactate (17%), marine sediment (12%) and
sewage sludge (7%).
The microorganisms used in the MFCs were classified as pure
cultures, mixed cultures or a comparison of the two types. Pure
cultures represented the largest proportion, 51% of the studies, as
shown in Fig. 7. Mixed cultures were used in 34% of the articles
and a comparison between the two types of cultures occurred in
10 of the studies. Five percent of the articles did not specify the
type of culture. Fig. 5. Technology and range of application used in the selected articles.
836 E.G. Ferreira Mercuri et al. / Renewable and Sustainable Energy Reviews 65 (2016) 832–840

GDP). However, the dominance in the number of published articles

is not merely a consequence of the percentage of investment made
by governments and private companies, but also an outcome of
the country's specific interest in the subject and the total amount
of money invested in MFC development. When you compare the
US to Japan, for example, Japan has a larger percentage of its GDP
in investment (3.4%) but a smaller number of articles than the US.
Brazil has no published articles and almost 3 times more invest-
ment in R&D than Belgium with 5 publications. Moreover, the
percentage of GDP in Belgium that is invested in research is twice
that of Brazil. It is evident, nevertheless, that there is a high cor-
relation between lower investment in R&D and fewer publications
per country. When comparing continents, Asia clearly has the
greatest potential, with 42 publications, overcoming America with
Fig. 6. Types of substrates used in the aqueous solution of MFCs. 23 articles. A different study about the scientific impact of nations
shows that US heads the list of nations in the volume of publica-
tions and citations and the share of top 1% most cited papers [31]
in all areas of WoS.
The results concerning the MFC's range of application confirm
that it is a new technology, still restricted to laboratories. Never-
theless, it is considered a promising source of bioenergy for the
future. The difficulty in increasing the size and capacity of the cells
is still a technological barrier to be overcome, although there are
articles reporting successes in industrial applications [28–30].
There is great potential for the generation of electricity with
MFCs associated with sewage treatment. Together, wastewater
sludge and domestic and industrial wastewater were cited in
65% of surveyed items. This is because the wastewater contains
many organic matter degrading microorganisms, such as Es-
cherichia coli and Pseudomonas aeruginosa, which are well
known to generate electricity. Wastewater treatment demands a
large amount of electricity and is an essential service for human
Fig. 7. Microorganism culture types used in MFC biofilms and studies showing the
comparison of pure cultures and communities. and environment health, therefore, making this process more
efficient and less expensive becomes mandatory. Moreover,
there is potential for the application of MFCs in various types of
We found a total of 34 taxa of microorganisms used in MFCs in industries, given the diversity of fluids with identified industrial
our survey. The two most cited (34% of the studies) were Geobacter origins, especially in the food industry, which produce effluents
sulfurreducens and Pseudomonas aeruginosa. The genus Shewanella rich in Glucose, Lactate and Maltose, cited by 47% of the articles.
appeared with 3 different species, plus one lineage (Fig. 8). Es- This is very relevant in huge, emergent and megadiverse coun-
cherichia coli, the most common microorganism in sewage, ap- tries such as Brazil and China.
peared in 3% of the studies. A large number of microorganisms (i.e. Some works report that the use of mixed cultures is more ef-
18 taxa) were not identified in previous reviews. ficient than single species because community resilience is in-
creased with better microenvironment interactions [9]. However,
in our survey the use of pure cultures is predominant. We believe
4. Discussion that greater attention should be placed on studies with mixed
cultures. Instead of the few articles found comparing axenic and
Our results indicate that MFC research is an emergent field, mixed cultures, 10% of the sample, they represent a good way to
since 2008 represents a significant breakthrough for the field in actually compare which species or communities are most effective
comparison to other research areas, with a considerable growth in for generating electricity in MFCs. In ecology, for example, many
the number of publications. One possible historical explanation for community and ecosystem studies support with strong evidence
such increase is the worldwide concern about global warming, that biodiversity increases the stability and resistance of numerous
sustainability and waste reuse, legally formalized in the Rio De- ecosystems [e.g. [32–34]].
claration on Environment and Development (1992) and the im- The two most used species are Geobacter sulfurreducens and
plementation of the Kyoto Protocol in 2005. In general, we ex- Pseudomonas aeruginosa. This result corroborates the findings of
pected an increasing number of studies after 2000, since the many reviews about the microorganisms used in MFCs published
number of new journals and the number of papers available on the in recent years [9,18,27]. Fig. 8 shows that the variety of species of
scientific databases have naturally increased and because MFCs microorganisms capable of generating electricity in MFCs is far
represent a new form of emergent, renewable and sustainable greater than those cited in other reviews on the subject
energy [7–10]. Furthermore, state of the art revisions on the sub- [6,18,27,35]. Many species appeared in only one article, indicating
ject were published between 2005 and 2008 [15,16,18,20]. a lack of understanding in the behavior of such species and great
The number of publications by country indicates that United opportunities for new research to fill these gaps in the future. We
States, South Korea, Japan and China hold the lead in MFC research hope that the increase in interdisciplinary collaborative research
when compared to the other nations. Our results also show that concerning biodiversity and its usage will increase the real appli-
the US dominates the subject and that the dominance is correlated cations of MFCs to improve sustainable energy on a large scale in a
to the amount of R&D investment made in this country (2.8% of the near future.
 E.G. Ferreira Mercuri et al. / Renewable and Sustainable Energy Reviews 65 (2016) 832–840 837

Fig. 8. Species used for the generation of electricity MFCs. The percentage utilization of each species is marked along the radial axis. The solid line indicates the 34 taxa
identified in our study. The dashed line indicates the 16 taxa mentioned in other reviews of microorganisms in MFCs [10,15–20].

5. Conclusion sustainable development of a country [31], especially huge and

emerging nations. When we turn our attention to renewable en-
We showed that in the past 17 years, the year 2008 represented ergy sources and energy crisis, in particular, we are increasingly
a significant breakthrough for research into MFCs in comparison to aware of the sorts of threats for which governments will need to
other research areas, with a considerable growth in the number of turn to their scientists. Taken together, our results can help re-
publications. The gaps are primarily related to the still limited search and application in this field on a global perspective.
number of species employed in studies and to the technological
barriers associated with moving from a laboratory to an industrial
scale. However, the growing number of publications on the subject Acknowledgements
in recent years is an indication that there is scientific effort to fill
such gaps. The two outstanding journals in the field, according to We are particularly grateful to the members of the Ecology and
relative weight, were MBT and JMB. Concerning the global dis- Conservation Laboratory (LEC) and Computer and Technology Lab
tribution of publications, the United States and East Asia are the in Environmental Engineering (LACTEA) of the Federal University
most promising locations for the development of MFCs, given both of Paraná (UFPR), who contributed significantly in preparing this
the number of publications and the amount of financial invest- manuscript. We thank James Nienow for English review, as well as
ment in research and development in these regions. Our results anonymous reviewers that evaluated and improved our manu-
show that there is a wide variety of microorganisms capable of script. CNPQ-Brazil provided grants to J.R.S.V.
generating electricity in MFCs, although the great majority of pa-
pers focus on few already well-established species. The main
technological barrier to the wide-spread use of MFCs is the scale of Appendix
application, which is still primarily restricted to small prototypes,
insufficient to generate electricity for practical purposes. The most Here we present the list of the 98 records included in the
cited substrate shows the great potential of MFCs in both power systematic review, which met the inclusion criteria during the
generation and wastewater treatment. It is clear that the size of a third and final screening of our study [36–133].
country's investment in R&D influences the number of articles
published by its researchers. The greater is the availability of fi-
nancial resources and interests of the country in this field, greater
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