Abstract
The development of products from marine bioresources is gaining importance in the biotechnology sector. The global market for Marine Biotechnology products and processes was, in 2010, estimated at € 2.8 billion with a cumulative annual growth rate of 5–10% (Børresen et al., Marine biotechnology: a new vision and strategy for Europe. Marine Board Position Paper 15. Beernem: Marine Board-ESF, 2010).
Marine Biotechnology has the potential to make significant contributions towards the sustainable supply of food and energy, the solution of climate change and environmental degradation issues, and the human health. Besides the creation of jobs and wealth, it will contribute to the development of a greener economy. Thus, huge expectations anticipate the global development of marine biotechnology.
The marine environment represents more than 70% of the Earth’s surface and includes the largest ranges of temperature, light and pressure encountered by life. These diverse marine environments still remain largely unexplored, in comparison with terrestrial habitats. Notwithstanding, efforts are being done by the scientific community to widespread the knowledge on ocean’s microbial life. For example, the J. Craig Venter Institute, in collaboration with the University of California, San Diego (UCSD), and Scripps Institution of Oceanography have built a state-of-the-art computational resource along with software tools to catalogue and interpret microbial life in the world’s oceans. The potential application of the marine biotechnology in the bioenergy sector is wide and, certainly, will evolve far beyond the current interest in marine algae.
This chapter revises the current knowledge on marine anaerobic bacteria and archaea with a role in bio-hydrogen production, syngas fermentation and bio-electrochemical processes, three examples of bioenergy production routes.
A.J. Cavaleiro and A.A. Abreu contributed equally to this chapter.
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Keywords
- Microbial Fuel Cell
- Hydrothermal Vent
- Dark Fermentation
- Microbial Electrolysis Cell
- Marine Biotechnology
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
1 Introduction
Energy is essential for life and has been a critical and decisive factor for the development of human civilizations. The ever-increasing use of energy, and particularly the overexploitation of fossil fuels and the depletion of easily accessible oil resources, have prompted several environmental problems and pressed the search for alternative renewable energy sources.
Renewable and sustainable bioenergy can be produced from any organic material that stored sunlight in the form of chemical energy. This includes lignocellulosic biomass, crops, agricultural and animal wastes, organic fraction of municipal solid wastes and some industrial organic wastes. Heat and electricity can be generated from these materials, as well as several liquid and gaseous biofuels, namely bioethanol, biobutanol, biodiesel, biogas and biohydrogen.
Chemical, thermo-chemical and biological technologies are currently used for biofuel production. Among these, processes performed by microorganisms are the most cost effective (Barnard et al. 2010). Nevertheless, a more comprehensive understanding of the microbial processes involved and the identification of novel microorganisms capable of producing biofuels is needed for process development and optimization.
Marine habitats are particularly attractive for bioprospection, due to the vast microbial abundance and diversity. Microorganisms that grow in deep oceanic environments have unique characteristics, necessary for thriving under extreme conditions of light, temperature and pressure. Therefore, the oceans contain an immense pool of genetic information with high biotechnology potential (Børresen et al. 2010).
Studies in deep oceans are technically challenging and expensive, but recent advances in genome sequencing techniques, metagenomics, remote sensing of microorganisms and bioinformatics have contributed to the intensification of marine biotechnology. This has resulted in different applications with societal importance, such as new therapeutics, chemical products and enzymes (Glöckner et al. 2012). Several genes of marine organisms have been patented and are mainly applied in pharmacology and human health (55%), agriculture or aquaculture (26%) and food industry (17%) (Arrieta et al. 2010). Applications in ecotoxicology, bioremediation and biofuel production are now emerging.
Marine non-phototrophic anaerobic microorganisms present an extensive and almost unexplored potential for biofuels production. The microbial communities present in hydrothermal fields use the energy of organic compounds (e.g. decaying biomass) but also reduced inorganic compounds (e.g. carbon monoxide) for growth, producing hydrogen, methane and alcohols (Sokolova et al. 2001). In the last decades, several hydrogen-producing bacteria have been screened from different marine environments, although few could be cultivated in the laboratory (Jayasinghearachchi et al. 2010). The use of extremophiles as catalysts may improve hydrogen yields in dark fermentation processes or the energy yield in microbial electro-chemical processes, since these microorganisms possess unique metabolic and physiological characteristics (Mathis et al. 2008).
In this chapter, the current knowledge on anaerobic microorganisms, or microbial cultures, retrieved from marine habitats with potential application in biotechnology systems for bioenergy production are reviewed, specially focusing on (1) dark fermentation for hydrogen production, (2) syngas (CO, CO2, H2) fermentation, and (3) electro-chemical processes (Fig. 18.1).
1.1 The Marine Environment
The marine environment covers more than 70% of the Earth’s surface and comprises 97% of all the water on the planet, much of which (75% of the ocean’s volume) at depths higher than 1,000 m. The ocean’s average depth is 4,000 m, but it may reach 11,000 m deep. The pelagic zone (from the Greek “open sea”) can be divided into several ecological sections based on depth (Fig. 18.2). The photic zone of the ocean, i.e. the volume actually penetrated by sunlight, is located in the upper layer, 200–300 m deep, and accounts only for approximately 2% of the total water volume. Therefore, the majority of the ocean (approx. 1.3 × 1018 m3) is deprived of light (Orcutt et al. 2011).
Besides the ocean water column, the marine environment includes other microbial habitats, namely marine sediments, the oceanic crust and hydrothermal vents. These environments are characterized by extreme pressure and temperature conditions (Fig. 18.2).
Pressure increases approximately 0.1 atm m−1 of water column, and more than 62% of the ocean is exposed to pressure values higher than 100 atm (Orcutt et al. 2011). Barophilic or piezophilic microorganisms exhibit an optimal growth at pressure higher than 400 atm, while barotolerant microorganisms have their optimal growth at pressures below 400 atm. Inhibitory effects of increased pressure on biochemical processes have been reported, and deep-sea microorganisms present specific features that allow them to live and grow under these high-pressure conditions (Horikoshi 1998; Kato and Bartlett 1997).
Temperature in the water column decreases from the surface until 100 m deep, from which it remains more or less constant around 2–4°C (Fig. 18.2). In hydrothermal vents, however, thermophilic and hyperthermophilic conditions are present and temperatures up to 400°C may occur (Orcutt et al. 2011). In these geological places, chemically reduced compounds are released at high temperatures from the earth subsurface. Mineral deposition occurs in these zones and may cause the formation of chimney structures surrounding the advecting fluids. Higher biological activity is present in these areas, relatively to the majority of the deep sea, with chemosynthetic archaea forming the base of a diverse food chain. Hydrogenotrophic methanogenesis and sulfate reduction are the dominant anaerobic processes in high temperature vent fluids (Orcutt et al. 2011).
The movement of chemical compounds (e.g. oxygen, nutrients, waste products) through the water column is another important factor that influences marine microbial communities. Caused by differences in temperature and salinity, vertical gradients occur in the water masses, creating zones with diverse physical and chemical characteristics. The metabolic activity of marine microorganisms is also greatly dependent on the availability and speciation of electron donors and acceptors. Organic matter and reduced inorganic compounds, such as hydrogen, methane, reduced sulfur compounds, reduced iron and manganese, and ammonium, are the main sources of electrons for the microbial metabolic reactions. Molecular hydrogen oxidation is energetically favorable, and thus marine microorganisms intensely compete for this compound (Orcutt et al. 2011).
Inorganic compounds such as oxygen, nitrate, nitrite, manganese and iron oxides, oxidized sulfur compounds and carbon dioxide may serve as electron sinks in marine microbial metabolisms (Table 18.1). The availability of terminal electron acceptors influences significantly the dominant microbial metabolic pathways. Microorganisms preferable use the electron acceptors that provide higher thermodynamic energy yields, generally following a redox cascade.
Microorganisms living in deep-sea habitats have different requirements in terms of salt concentration for growth. Halotolerant microbes prefer low salt concentration, but are able to survive and grow in the presence of relatively high Na+ concentrations, while halophilic microorganisms require salt concentrations from 0.5 to 2.5 M or even higher (saturated solutions) (Kivistö and Karp 2011).
1.2 Microbial Abundance and Diversity in the Marine Environment
The discovery of high microbial activity in deep ocean and sediments, previously considered devoid of life, significantly changed the understanding of marine ecosystems. In the last decades, genomic and metagenomic approaches and the use of high throughput sequencing techniques have revealed the remarkable diversity of marine microbes, and contributed to the identification of novel ecological processes and functions in the marine environments. Dedicated research programs were launched, specifically focusing on the assessment of genetic diversity and function in marine microbial communities. For example, the Global Ocean Sampling expedition (GOS) by Craig Venter started in 2004 with the aim of improving the number of whole genome sequences of ecologically relevant marine microorganisms (Sun et al. 2011).
Total number of bacteria and archaea in the ocean is estimated to be around 1029 cells. Prokaryotic biomass concentration in the pelagic zone is approximately 103–105 cells mL−1 and tends to decrease with depth, contrasting with diversity that typically is higher at higher profundities. In deep sediments microbial abundance exceeds 105 cells mL−1. In these habitats, higher abundance and diversity occur at the surface and then decrease sharply, reflecting changes in the geochemical characteristics of the sediments (Nagata et al. 2010; Orcutt et al. 2011; Zhang et al. 2012).
A relatively high abundance of Archaea (10–50% of total prokaryote cell abundance), has been reported in the bathypelagic communities (Nagata et al. 2010; Orcutt et al. 2011). The structure of these communities appears to be more closely related with depth than with the local of origin, since microbial communities collected in different places at the same depth present higher similarity than the microbial assemblages inhabiting a specific ocean at different depths. This fact suggests the existence of vertical stratification patterns at global scale (Orcutt et al. 2011).
Similar marine habitats appear to be dominated by similar microbial groups (at the phylum level) (Inagaki et al. 2006; Orcutt et al. 2011). Alpha-, Delta- and Gamma-Proteobacteria prevail in typical deep-ocean bacterial communities, whereas the Crenarchaeota marine group I dominates the archaeal communities (Eloe et al. 2011; Fuhrman and Davis 1997; Orcutt et al. 2011). In deep sediments, predominant phylotypes of the Archaea domain include the Crenarchaeota clades Marine Benthic Group B and Miscellaneous Crenarchaeota Group, for which there are no cultivated members. These habitats also include as dominant bacteria, members of the candidate OP9/JS1 phylum or of the Chloroflexi phylum (Inagaki et al. 2006; Orcutt et al. 2011; Schippers et al. 2012; Zhang et al. 2012). Gamma- and Epsilonproteobacteria dominate the hydrothermal habitats, as well as members of the Euryarchaeota phylum, from genera Archaeoglobus, Thermococcales and Methanococcales (Orcutt et al. 2011; Sokolova et al. 2001).
Despite the recent advances achieved with metagenomic approaches, an enormous pool of previously unknown, uncultured microorganisms and genes has been revealed. As an example, Venter et al. (2004) identified over 1.2 million previously unknown genes through genome shotgun sequencing of samples from the Sargasso Sea. The function of many of these genes was not identified thus far (Glöckner et al. 2012; Pedrós-Alió 2006). In order to fully exploit the genomic potential of marine microbes, with possible applications in biotechnology, the development of novel research tools for the characterization of these previously unknown marine microorganisms is absolutely necessary (Glöckner et al. 2012).
In line with this need, the J. Craig Venter Institute (JCVI) launched the project CAMERA, the Community Cyber Infrastructure for Advanced Marine Microbial Ecology Research and Analysis Database, which is a continually evolving open access tool for general access to raw environmental sequence data, associated metadata, pre-computed search results, and high-performance computational resources (http://camera.calit2.net/). The aim of this project is to serve the needs of the microbial ecology research community by creating a rich, distinctive data repository and a bioinformatics tools resource that will address many of the unique challenges of metagenomics analysis. Initially, CAMERA is making available all the metagenomic data being collected by the J. Craig Venter Institute’s Sorcerer II Global Ocean Sampling (GOS) expeditions, which have sampled microbial communities around the globe, plus 150 new full genome maps of ocean microbes. It also includes other data sets: a large-scale metagenomic survey of marine viral organisms collected from sites around the North American continent by Forest Rohwer and his research team at San Diego State University, and a vertical profile of marine microbial communities collected at the Hawaii Ocean Time-Series (HOTS) station ALOHA by Ed DeLong and his research team at Massachusetts Institute of Technology (MIT) (http://www.jcvi.org/cms/research/projects/camera/overview/).
2 Dark Fermentation Process
Hydrogen, a high-energy, non-polluting and environmental friendly compound can be biologically produced through biophotolysis, indirect biophotolysis, photofermentation and dark fermentation of organic matter. In dark fermentation, carbohydrate-rich substrates are converted by anaerobic microorganisms into organic acids and alcohols, releasing hydrogen and CO2 in the process. A variety of microorganisms can be involved in this process, either as pure or in mixed cultures.
This process has several advantages relatively to other biological hydrogen production methods, namely the use of a wide range of organic substrates, including organic wastes, and higher hydrogen production rates (Hallenbeck et al. 2012). However, the economical feasibility of dark fermentation still needs to be improved, for example through technological developments and increased knowledge on microorganisms capable of efficient hydrogen production.
In dark fermentation, strictly anaerobic or facultative microorganisms break down complex organic matter under anaerobic conditions, producing organic acids and alcohols, and releasing H2 and CO2. Carbohydrates are hydrolyzed to monomeric simple sugars, that are further converted to acetyl-coenzyme A (acetyl-CoA) mainly through pentose phosphate and glycolysis pathways (Fig. 18.3).
The maximum theoretical yield of fermentative hydrogen production is 4 mol H2 mol−1 hexose, estimated from the reaction of glucose conversion to acetate. The production of pyruvate from glucose yields 2 moles of reduced nicotinamide adenine dinucleotide (NADH), which can be regenerated with the formation of 2 mol of hydrogen (Fig. 18.3). Further breakdown of pyruvate generates acetyl-CoA and reduced ferredoxin (Fdred). Re-oxidation of ferredoxin yields hydrogen (1 mol H2 mol−1 Fd), making a total hydrogen yield of 4 moles per mol of glucose consumed.
Alternative pathways for hydrogen production have also been reported in microorganisms isolated from marine habitats, such as Vibrio aerogenes and Pantoea agglomerans (Shieh et al. 2000; Zhu et al. 2008), although yielding lower amounts of hydrogen (around 2 mol H2 mol−1 hexose).
Fermentative hydrogen production can be carried out by a wide range of marine microorganisms, with diverse requirements in terms of substrate preference, pH and temperature (Wang and Wan 2009). Those parameters do not only determine the growth of the microorganisms, but also have a crucial role on the metabolic pathway that will prevail, severely affecting the final hydrogen yield (Table 18.2). Another important parameter, with significant influence on hydrogen production, is hydrogen partial pressure (PH2). High PH2 tend to divert the metabolic pathway towards more reduced end products (e.g. lactate and ethanol), with consequently lower H2 yields. However, at higher temperatures this effect is not so severe. For example, at 25°C, PH2 needs to be lower than 0.022 kPa to allow for the conversion of glucose to acetate (reaction 2 in Table 18.2), while at 100°C this reaction becomes exergonic at PH2 lower than 2.2 kPa (Verhaart et al. 2010).
Several archaea and bacteria capable of efficient hydrogen production were isolated from marine environments, mostly from hydrothermal vents and deep-sea geothermal heated sediments (Table 18.3). These microorganisms grow at very high temperatures (extreme thermophilic and hyperthermophilic), with enhanced hydrolysis and thermodynamically more favorable metabolic reactions (Verhaart et al. 2010). This high potential for biotechnology applications has been explored at lab-scale, mainly in batch or fed-batch conditions, as shown in Table 18.3.
Clostridium amygdalinum grows at mesophilic temperatures between 20 and 60°C, with an optimum around 45°C. These spore-forming anaerobic aerotolerant bacteria are able to tolerate and grow in the presence of up to 50% air in the gas phase (Parshina et al. 2003). Thermotoga species are marine microorganisms that are able to produce hydrogen and grow at temperatures up to 80°C (Frock et al. 2010).
The anaerobic archaea reported in Table 18.3 belong to the order Thermococcales that include two major genera, Thermococcus and Pyrococcus. Thermococcus kodakaraensis and Thermococcus onnurineus grow between 60 and 100°C. Pyrococcus furiosus grows at 70–103°C with an optimum around 100°C. A fast doubling time of 37 min was reported for this microorganism. This fermentative anaerobe is capable of utilizing maltose, starch, glycogen or cellobiose (Fiala and Stetter 1986).
As shown in Table 18.3, hydrogen yields around 3–4 mol H2 mol−1 hexose were obtained for the different microorganisms and substrates tested. Maximum hydrogen yields were achieved in pure cultures of Thermotoga species (Table 18.3), probably related to a bifurcating hydrogenase. This hydrogenase, recently characterized in T. maritima (Schut and Adams 2009), uses the reducing equivalents from both NADH and reduced ferredoxin in a 1:1 ratio to produce hydrogen. Ferredoxin oxidation is thermodynamically unfavorable at standard temperature and pressure conditions (∆G 0′ = +3 kJ reaction−1), but becomes exergonic for low PH2 (e.g. ∆G′ = −25 kJ reaction−1 for PH2 = 1 Pa) (Abreu et al. 2012). Apparently, the exergonic oxidation of ferredoxin is used to drive the unfavorable oxidation of NADH. To maintain the 1:1 ratio of reducing equivalents from Fd and NADH, T. maritima seems to use a Fd:NADH oxireductase to supply the bifurcating hydrogenase.
Recently, the genome of several of these microorganisms has been sequenced (Fukui et al. 2005), providing new information and allowing the discovery of novel functions. For example, the genome sequencing of Thermococcus onnurineus allowed the identification of genes coding for multiple hydrogenases (Lee et al. 2008). The genome sequencing data of T. maritima DSM 3109 showed the presence of numerous metabolic pathways involved in the degradation of many simple and complex carbohydrates, namely glucose, xylose, mannose, starch, carboxymethylcellulose (CMC), xylan, and pectin (Huber et al. 1986). Moreover, 8–11% of T. maritima genes were found to be most similar to Archaea, whereas 42–48% of genes were most similar to Firmicutes, suggesting the occurrence of lateral gene transference between these microbial groups (Nelson et al. 1999). This mechanism may contribute to the development of new capacities by marine bacteria, improving the ability to live in extreme habitats and cope with environmental changes.
With genomic information, chromosomal gene disruption or replacement technology can be applied to expand the range of substrates utilized, as well as to knockout competitive metabolic pathways or increase species resilience. For instance, T. kodakaraensis KOD1 cannot utilize maltose as a carbon source because of the lack of maltose transporter (Fukui et al. 2005). Introduction of the genes encoding the respective transporter of other hyperthermophiles (such as P. furiosus and T. litoralis (DiRuggiero et al. 1999)) could develop a new strain with the ability to produce H2 from maltose.
3 Syngas Fermentation
In the last decades, the biological process of synthesis gas fermentation has gained interest as a sustainable technology for the production of valuable compounds and biofuels, namely methane, ethanol and butanol. Low biodegradable materials, such as lignocellulosic components of biomass, and other recalcitrant wastes (e.g. naphta, residual oil and petroleum coke) are used as substrate for syngas production through gasification (Ragauskas et al. 2006; Lawson et al. 2011). This process is performed at temperatures higher than 700°C with controlled supply of oxygen and/or steam. Formed syngas is mainly composed of CO, CO2 and H2 (McKendry 2002). Syngas can be further converted to fuels, either through catalytic processes (e.g. Fischer-Tropsch for olefins and gasoline synthesis) (Spath and Dayton 2003) or microbial processes.
Biological processes, although generally slower than chemical reactions, have several advantages over chemically catalyzed processes, such as higher specificity, higher yields, and generally greater resistance to poisoning (Klasson et al. 1992). These microbiological reactions occur at moderately high temperature and pressure conditions, resulting in minimum energy requirements and comparative lower cost.
Acetogenic anaerobes oxidize CO to CO2 and H2 via CO dehydrogenase (CODH) through a water-gas shift reaction (reaction 6 in Table 18.4). CODH is linked to the Wood-Ljungdahl pathway (or reductive acetyl-CoA pathway), which plays a central role in acetogenic CO metabolism (Fig. 18.4). In this pathway, H2 (or CO) is used as an electron donor and CO2 as an electron acceptor, with the formation of acetyl-Coenzyme A (acetyl-CoA) (Fischer et al. 2008). Alternatively, hydrogen and CO2 can also react to form CO, which is further converted to acetyl-CoA via acetyl-CoA synthase system, by the activity of a CO dehydrogenase (Kopke et al. 2010). Acetyl-CoA is the precursor of volatile fatty acids (e.g. acetate, butyrate) and alcohols, namely ethanol and butanol. Therefore, Wood-Ljungdahl pathway represents a possible alternative to glycolysis in the formation of this precursor, and gasification of biomass constitutes a more direct pathway towards the production of acetyl-CoA (Fig. 18.4).
Additionally, the different syngas components (CO, H2 and CO2) can be biologically converted to methane (CH4), as show in reactions 11, 12 and 13 in Table 18.4. Methanogenesis is a biological process performed by prokaryotic microorganisms from the Archaea domain, observed in a wide range of environments, such as oceans, lakes, sediments, hydrothermal vents, anaerobic bioreactors and human and animal gut (Sowers and Ferry 2003).
CO utilization seems to be a quite widespread feature distributed among different phyla of bacteria and archaea (Henstra et al. 2007a). The presence of CO-consuming anaerobic microorganisms was detected in sediments and hydrothermal vents, where CO is one of the main components (e.g. Svetlichny et al. 1991). The number of carboxydotrophic isolates retrieved from marine environments is relatively low (Table 18.5), but considering the microbial diversity in CO-containing environments this number is probably underestimated.
One of the reported CO-consuming microorganisms isolated from submarine hot vent is the Caldanaerobacter subterraneus (Table 18.5). This Gram-positive, non-motile bacterium grows chemolitotrophically on CO with the production of equimolar quantities of CO2 and H2. C. subterraneus is an extreme-thermophile with optimum growth temperature at 70°C, belonging to Clostridia class. Another bacterium, Acetobacterium woodii, is capable of utilizing CO or H2 + CO2 at 30°C with the formation of acetate. A. woodii is a Gram-positive bacterium with oval-shaped cells, and was isolated from marine sediments (Balch et al. 1977).
The first carboxydotrophic archaea described was isolated from hydrothermal vents and belongs to the Thermococcus genera (Sokolova et al. 2004). Thermococcus strain AM4 presents coccoid cells and grows at hyperthermophilic conditions (80°C), producing H2 and CO2 from CO (Table 18.5). Thermococcus onnurineus is also able to grow in media supplemented with carbon monoxide, producing H2 (Lee et al. 2008). A maximum hydrogen production rate of 1.55 mmol H2 L−1 h−1 and a yield of 0.98 mol H2 mol−1 substrate were obtained from the degradation of CO in batch bioreactors inoculated with pure culture of T. onnurineus (Bae et al. 2012). Complete genome sequencing of this microorganism allowed the identification of genes coding for a CO dehydrogenase (Codh) (TON_1018), besides multiple hydrogenases (Lee et al. 2008).
Carbon monoxide is also utilized by Archaeoglobus fulgidus, a hypherthermophilic archaea (optimal growth at 83°C) with irregular coccoid cells, isolated from submarine hot spring. A. fulgidus can grow chemolitoautotrophically with CO forming acetate (Henstra et al. 2007b).
The mesophilic Methanosarcina acetivorans, isolated from marine sediments, and the hyper-thermophilic Methanocaldococcus jannaschii, isolated from hydrothermal vent, can utilize CO for the formation of methane. Additionally, these archaea can also convert H2 + CO2 to methane.
Other marine archaea are able to produce methane from the gaseous mixture of CO2 and H2 (Sowers and Ferry 2003). Mesophilic and extreme-thermophilic microorganisms were isolated from sediments and hydrothermal vents, respectively. These microorganisms mainly belong to the genera Methanococcus, Methanocaldococcus, Methanoculleus, Methanolacinia, Methanogenium and Methanopyrus (Sowers and Ferry 2003).
Despite the high potential of marine microorganisms for bioenergy production from syngas through biological fermentation, this process is still not sufficiently studied. Practical applications in biotechnological process have just emerged, requiring further research for full exploitation of its potential.
4 Electro-Chemical Processes
Harvesting electrons from bacterial metabolism as a potential sustainable energy source has been for long subject of research interest, but only in the last few years the prospects for practical applications improved considerably due to the development of microbial fuel cells (MFC) with enhanced power output (Liu et al. 2004; Liu and Logan 2004; Rabaey et al. 2003, 2004).
In a MFC, biological and electrochemical processes are combined to convert dissolved organic matter directly into electrical current. This is achieved by diverting the electrons produced by electrochemically active bacteria, during oxidation of the organic matter, towards an insoluble acceptor, i.e. the anode electrode. The produced protons diffuse through a membrane into a cathode compartment, where they react with oxygen generating water and an electrical current from the anode towards the cathode. In general, a MFC is a two-chamber structure, one containing the anode and electrochemically active bacteria growing under anaerobic conditions, and another containing the cathode (Fig. 18.5). The cathode chamber is kept aerobic by sparging air in the water. Simplified designs were developed with single-chamber configurations where the cathode is fused to the proton exchange membrane and directly exposed to air (Liu et al. 2004; Liu and Logan 2004; Park and Zeikus 2003). Simple systems without proton exchange membranes have been developed as well (Liu et al. 2005; Liu and Logan 2004). The performance of the MFC depends on several parameters, such as substrate conversion rate, performance of the proton exchange membrane and internal resistance of the MCF (Rabaey and Verstraete 2005).
A diverse range of microorganisms has been found capable of interacting with electrodes, usually referred as anodophiles (Park and Zeikus 2003), exoelectrogens (Logan and Regan 2006), electrogenic (Debabov 2008), anode-respiring (Torres et al. 2007) or electrochemically active microorganisms (Chang et al. 2006). The term electricigens was also proposed specifically for microorganisms that completely oxidize organic compounds to carbon dioxide with an electrode serving as the sole electron acceptor (Lovley 2006). Several mechanisms by which microorganisms may transfer electrons to the anode of microbial fuel cells have been proposed, including direct electron transfer through outer-surface c-type cytochromes (Busalmen et al. 2008), conductive biofilm matrix containing cytochromes (Marcus et al. 2007) or microbial nanowires (Reguera et al. 2005), and indirect electron transfer through soluble electron shuttles (Marsili et al. 2008).
Microbial fuel cells were first developed to produce power from the electrical current generated by bacteria, but there has been an evolution of the system for other applications. Additional voltage added to the potential generated by the bacteria allow for various products to be generated at the cathode, such as hydrogen (Rozendal et al. 2006), methane (Cheng et al. 2009) and hydrogen peroxide (Rozendal et al. 2009). The terms bio-electrochemical systems (BES), microbial electrolysis cell (MEC) and microbial electrochemical systems (MxC) have been used to describe those technologies. Other applications include sensoring, remediation and wastewater treatment (Clauwaert et al. 2007; Li et al. 2008; Liu et al. 2004; Liu and Logan 2004; Tront et al. 2008; Zhang et al. 2010).
The first practical application of marine microbial fuels cells was to power low-energy consuming marine instrumentation, e.g. meteorological buoys capable of measuring air temperature, pressure, relative humidity and water temperature (Tender et al. 2008). Anaerobic marine MFC are generally composed of graphite electrodes that are placed in situ: the anode is introduced in anaerobic marine sediments and the cathode is positioned in the oxygen-rich seawater (Fig. 18.5). The naturally occurring microorganisms colonize the anode and oxidize the organic substrates present in the sediments, while in the cathode seawater constituents are reduced. These systems are based on the natural redox gradient that occurs at the water-sediment interface due to the microbial metabolic activity, and do not require proton exchange membrane (Dumas et al. 2007; Tender et al. 2002). Addition to the sediments of insoluble slowly degrading organic substrates, such as chitin or cellulose, or the use of anodes modified with charge transfer mediators, has resulted in power output increase (Rezaei et al. 2007, 2008, 2009). For example, Lowy and Tender (2008) reported a maximum power density of approximately 98 mW m−2 (of anode area) at a cell voltage of 0.24 V in a marine MFC operating with an anthraquinone-1,6-disulfonic acid (AQDS)-modified graphite anode, while a maximum value around 20 mW m−2 at 0.30 V was attained in a similar system assembled with a plain graphite anode.
Anoxic marine sediments have been frequently used as source of electrogenic microorganisms (Table 18.6). Sequences from a denaturing gradient gel electrophoresis (DGGE)-screened 16S rDNA clone library showed that a marine sediment used to inoculate an MFC fed with cysteine resulted in a bacterial community in which 97% of the sequences detected belong to the Gammaproteobacteria and were similar to Shewanella affinis KMM 3686 (40% of clones), with Vibrio spp. and Pseudoalteromonas spp. being the next most frequently detected (Logan et al. 2005).
The Shewanella genus has a wide environmental distribution and several species have been retrieved from marine and freshwater habitats. These mesophilic facultative anaerobic bacteria are capable of dissimilatory metal reduction (DMR). Member of the genus Shewanella grow forming a biofilm on insoluble metal oxides, which facilitates the contact between bacteria and the metal allowing direct electron transfer. Alternative mechanisms of electron transfer by Shewanella (nanowires or soluble electron shuttles) have also been proposed (Flynn et al. 2012; Venkateswaran et al. 1999). Pure cultures of Shewanella oneidensis DSP10 and Shewanella oneidensis MR-1 were used as inocula for power generation from lactate in marine sediment MFC (Kim et al. 2002; Ringeisen et al. 2006). High output power per device cross-section and volume (3 W m−2, 500 W m−3, respectively) was achieved in a miniature microbial fuel cell (mini-MFC) inoculated with Shewanella oneidensis DSP10. Current and power was enhanced 30–100% by the addition of electron mediators (Ringeisen et al. 2006). The genome of this bacterium was completely sequenced in 2002, contributing for the understanding of the mechanisms involved in Shewanella metabolism (Heidelberg et al. 2002).
Other studies report a clear dominance of Deltaproteobacteria in sediment MFC. Bond et al. (2002) verified that 71% of the sequences obtained in a 16S rDNA clone library from an anode electrode were Deltaproteobacteria, and 70% of these belonged to the family Geobacteraceae. In a similar system, Deltaproteobacteria accounted for 76% of the sequences retrieved, from which 59% were from the family Geobacteraceae and presented more than 95% similarity to Desulfuromonas acetoxidans (Tender et al. 2002). Another group of Deltaproteobacteria sequences, most closely related to sulfate-reducing bacteria from the family Desulfobulbaceae, was also consistently enriched on the anodes of marine sediment fuel cells (Holmes et al. 2004a). In fact, in one field experiment, organisms in this cluster accounted for all of the deltaproteobacterial sequences and for approximately 62% of the bacterial 16S rRNA gene sequences recovered from the current-harvesting anode (Holmes et al. 2004a).
Desulfuromonas acetoxidans, from the Desulfuromonadacea family of Deltaproteobacteria, was isolated from Antarctic Ocean marine sediments and is a strictly anaerobic, rod-shaped, Gram-negative bacterium (Pfennig and Biebl 1976). In this bacterium, the complete oxidation of organic compounds, such as acetate, ethanol or propanol, is coupled with the reduction of a wide range of soluble and insoluble electron acceptors (e.g. sulfur, fumarate, ferric iron or manganese) (Table 18.6). Electron transfer to the anode appears to be related with a complex network of multiheme cytochromes, from which only few have been characterized (Alves et al. 2011). Despite the reported abundance of D. acetoxidans in microbial communities colonizing the anode of sediment MFC (e.g. Tender et al. 2002), inoculation of MFC with pure cultures of these microorganisms has not been tested.
Several mesophilic psychrotolerant bacteria, capable of DMR metabolism, have been isolated from marine sediment MFC, namely Geopsychrobacter electrodiphilus, Prolixibacter bellariivorans, Rhodoferax ferrireducens (Finneran et al. 2003; Holmes et al. 2004b, 2007). These mesophilic microorganisms can grow and reduce metals, e.g. iron(III), manganese (IV), at low temperatures (ca. 4°C), although exhibiting optimum growth around 22–25°C. Lab-scale experiments were performed with MFC inoculated with a pure culture of Rhodoferax ferrireducens, achieving electric current intensity of 31 mA m−2 (Chaudhuri and Lovley 2003). Higher values of electric current (209–254 mA m−2) were obtained at 60°C with a MFC prepared with a thermophilic electrogenic microbial community recovered from marine sediments (South Carolina, USA) (Mathis et al. 2008). The main ribotype retrieved (approximately 68% of the clones) was found to be closely related to Thermincola carboxydophila (99% similarity), with uncultured microorganisms belonging to the Firmicutes and Deferribacteres phyla as the remaining 16S rRNA genes.
In the last years MFC systems have developed considerably toward a simple and robust technology. The main research efforts have been focused on the materials and configuration of electrodes and proton exchange membranes, as well as the design of the MFC system. More inputs on the selection of electricigenic microbial communities are required for optimal electricity production in MFC. Marine environments constitute a powerful source of potential electrochemically active microorganisms.
5 Conclusions and Future Prospects
Marine habitats can offer unique microbial and metabolic features with huge potential for application in bioenergy production processes. Dark fermentation, syngas fermentation and bioelectrochemical processes were selected as demonstration examples of the potential application of marine anaerobic bacteria and archaea in the bioenergy field.
The advances in “omics” in line with newly designed and optimized biotechnology processes, for example operating at extreme conditions of temperature and pressure or electrically assisted, will turn marine biotechnology a field of growing interest and increasing application in the sector of bioenergy.
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Cavaleiro, A.J., Abreu, A.A., Sousa, D.Z., Pereira, M.A., Alves, M.M. (2013). The Role of Marine Anaerobic Bacteria and Archaea in Bioenergy Production. In: Malik, A., Grohmann, E., Alves, M. (eds) Management of Microbial Resources in the Environment. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5931-2_18
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