TY - JOUR
AU - Bose, Arpita
AB - Abstract Microbial electron uptake (EU) is the biological capacity of microbes to accept electrons from electroconductive solid materials. EU has been leveraged for sustainable bioproduction strategies via microbial electrosynthesis (MES). MES often involves the reduction of carbon dioxide to multi-carbon molecules, with electrons derived from electrodes in a bioelectrochemical system. EU can be indirect or direct. Indirect EU-based MES uses electron mediators to transfer electrons to microbes. Although an excellent initial strategy, indirect EU requires higher electrical energy. In contrast, the direct supply of cathodic electrons to microbes (direct EU) is more sustainable and energy efficient. Nonetheless, low product formation due to low electron transfer rates during direct EU remains a major challenge. Compared to indirect EU, direct EU is less well-studied perhaps due to the more recent discovery of this microbial capability. This mini-review focuses on the recent advances and challenges of direct EU in relation to MES. Introduction Oxidation–reduction reactions are responsible for energy transformations by nearly all life-forms. Most organisms use soluble oxidants and reductants as electron-acceptors or -donors. Some microorganisms can, however, acquire energy through electron transfer to or from extracellular solid inorganic compounds, using them as electron-acceptors or -donors, respectively. This microbial metabolism is specifically termed as “extracellular electron transfer (EET)” [22, 24, 53]. EET is a widespread process in nature and is critical for biogeochemical cycling of various elements. In addition, EET has also been leveraged for a number of applications. EET plays an important role in bioelectrochemical systems and associated applications. These applications can be categorized mainly into (i) microbial fuel cells (MFC), (ii) microbial electrolysis cells (MEC), and (iii) microbial electrosynthesis (MES). MFCs are bioanode-driven systems, and they produce electricity by wiring a bioanode to a chemical cathodic reaction (O2 or ferricyanide) [23]. It involves EET from microbes to an electrode/anode. These microbes are often called exoelectrogens. This microbial ability has been utilized for various applications, such as bioremediation, energy generation and biosynthesis [23, 25, 36]. But MECs are perhaps equally, if not more important, for scaled applications. They also use a bioanode and rely on small energy input to set a differential voltage and make H2 at the cathode [1, 6]. In contrast, MES is a biocathode-driven approach, and it is a recently described bioelectrochemical process that uses microbes to produce biofuels or bioelectrocommodities from carbon dioxide (CO2) and electricity. It involves EET from an electrode/cathode (or from solid conductive materials such as iron minerals) to microbes [5, 39, 51]. This form of EET is also called microbial electron uptake (abbreviate this as EU throughout). EU-capable microbes are called “electrotrophs” and can consume electricity from electrodes or electrons from electroconductive solid materials to produce value-added multi-carbon products [43, 58]. Various studies have shown that MES can occur via either indirect or direct EU. In direct EU, microorganisms attach to solid electroconductive surfaces (cathodes or iron minerals) and directly take up electrons from them [5, 18, 32, 33, 41, 59] (Fig. 1). In contrast, during indirect EU, microorganisms indirectly acquire electrons from conductive materials using diffusible chemicals that are either produced electrochemically or added to the reactors [14, 19, 26, 29, 35, 47, 49, 52] (Fig. 1). Fig. 1 Open in new tabDownload slide a Schematic of extracellular electron uptake (EU) pathways adopted in microbial electrosynthesis (MES) at different poised cathode potentials (PCP) vs. standard hydrogen electrode (SHE). (M ox mediator oxidation, M rd mediator reduction, PHB polyhydroxybutyrate) The primary focus of this mini-review is to discuss the recent advances and challenges of direct EU from solid poised electrodes in MES as it is less well-studied than indirect EU. This mini-review provides examples where direct EU has been implicated for MES (Table 1). In addition, this mini-review is intended to highlight the fact that applications and mechanistic studies go hand-in-hand when studying microbe-charged surface interactions. Examples of direct microbial electron uptake (direct EU) by different electrotrophs for microbial electrosynthesis (MES) Microbial group . Electrotrophs . Application . PCP vs. SHE . Potential mechanism of EU/biological phenomenon noted . References . Acetogens Moorella thermoautotrophica, Moorella thermoacetica (thermophile) MES − 0.4 Temperature-dependent carbon dioxide (CO2) reduction to acetate via EU at 60 °C [15] Co-culture of Sporomusa ovata/Desulfobulbus propionicus MES NA Sulfide oxidation by D. propionicus. Electrons generated were then used by S. ovata to reduce CO2 to acetate on a graphite cathode [17] Sporomusa ovata MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate by S. ovata [33] Sporomusa silvacetica, Sporomusa sphaeroides, Clostridium ljungdahlii, Clostridium aceticum MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate [32] Methanogens Marine lithoautotrophic methanobacterium-like archaeon strain IM1 Electromethanogenesis − 0.4 Direct EU from graphite cathodes to convert CO2 to methane (CH4) without hydrogen serving as a cathode-generated electron carrier [2] Methabacterium palustre Electromethanogenesis − 1.0 Direct EU from the cathode to convert CO2 to CH4 [7] Methanococcus maripaludis (electromethanogenic archaeon) MES − 0.6 Surface-associated redox enzymes and formate dehydrogenases are involved in direct EU [30] Mixed methanogenic culture Electromethanogenesis − 1.5 Electrically reduced neutral red (NR) served as the sole source of reducing power for growth and metabolism of a mixed methanogenic culture in the MES system [34] Methanothermobacter thermautotrophicus Electromethanogenesis NA Applied voltage as a reducing power source to reduce CO2 to CH4 [45] Mixed methanogenic culture Electromethanogenesis − 0.456 Applied cathodic potential and environmental conditions are key factors for “electrometabolism” [46] Methanosaeta and Methanosarcina (acetoclastic methanogens) Electromethanogenesis − 0.7 Antibiotics pretreatment effectively inhibited hydrogen (H2)-utilizing methanogens and significantly promoted the growth of acetoclastic methanogens [54] Bioreactors enriched in Methanobacterium sp. methanogens Electromethanogenesis − 0.7 Multiple pathways of electron transfer, including direct cathode-to-cell, interspecies exchange, and semi-conductive conduits implicated [60] Photoautotrophic microbes Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 The pioABC operon that is essential for photoautotrophic growth by ferrous iron (Fe(II)) oxidation, influences direct electron uptake from the cathode [5] Green sulfur bacterium Prosthecochloris aestaurii with a heterotrophic partner bacterium Geobacter sulfurreducens No application explored (mechanistic study) − 0.401 Anoxygenic photosynthesis by P. aestaurii is driven by electrons derived either from a solid electrode or acetate oxidation via direct interspecies electron transfer (DIET) from G. sulfurreducens [18] Rhodopseudomonas palustris TIE-1 MES + 0.1 Intracellular accumulation of PHB with light as an energy source, poised electrodes as electron source (via direct EU) and CO2 as a carbon source [40] Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 Electrochemically deposited Prussian blue (PB) complex enhanced the direct EU by 3.8 times [41] Microbial group . Electrotrophs . Application . PCP vs. SHE . Potential mechanism of EU/biological phenomenon noted . References . Acetogens Moorella thermoautotrophica, Moorella thermoacetica (thermophile) MES − 0.4 Temperature-dependent carbon dioxide (CO2) reduction to acetate via EU at 60 °C [15] Co-culture of Sporomusa ovata/Desulfobulbus propionicus MES NA Sulfide oxidation by D. propionicus. Electrons generated were then used by S. ovata to reduce CO2 to acetate on a graphite cathode [17] Sporomusa ovata MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate by S. ovata [33] Sporomusa silvacetica, Sporomusa sphaeroides, Clostridium ljungdahlii, Clostridium aceticum MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate [32] Methanogens Marine lithoautotrophic methanobacterium-like archaeon strain IM1 Electromethanogenesis − 0.4 Direct EU from graphite cathodes to convert CO2 to methane (CH4) without hydrogen serving as a cathode-generated electron carrier [2] Methabacterium palustre Electromethanogenesis − 1.0 Direct EU from the cathode to convert CO2 to CH4 [7] Methanococcus maripaludis (electromethanogenic archaeon) MES − 0.6 Surface-associated redox enzymes and formate dehydrogenases are involved in direct EU [30] Mixed methanogenic culture Electromethanogenesis − 1.5 Electrically reduced neutral red (NR) served as the sole source of reducing power for growth and metabolism of a mixed methanogenic culture in the MES system [34] Methanothermobacter thermautotrophicus Electromethanogenesis NA Applied voltage as a reducing power source to reduce CO2 to CH4 [45] Mixed methanogenic culture Electromethanogenesis − 0.456 Applied cathodic potential and environmental conditions are key factors for “electrometabolism” [46] Methanosaeta and Methanosarcina (acetoclastic methanogens) Electromethanogenesis − 0.7 Antibiotics pretreatment effectively inhibited hydrogen (H2)-utilizing methanogens and significantly promoted the growth of acetoclastic methanogens [54] Bioreactors enriched in Methanobacterium sp. methanogens Electromethanogenesis − 0.7 Multiple pathways of electron transfer, including direct cathode-to-cell, interspecies exchange, and semi-conductive conduits implicated [60] Photoautotrophic microbes Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 The pioABC operon that is essential for photoautotrophic growth by ferrous iron (Fe(II)) oxidation, influences direct electron uptake from the cathode [5] Green sulfur bacterium Prosthecochloris aestaurii with a heterotrophic partner bacterium Geobacter sulfurreducens No application explored (mechanistic study) − 0.401 Anoxygenic photosynthesis by P. aestaurii is driven by electrons derived either from a solid electrode or acetate oxidation via direct interspecies electron transfer (DIET) from G. sulfurreducens [18] Rhodopseudomonas palustris TIE-1 MES + 0.1 Intracellular accumulation of PHB with light as an energy source, poised electrodes as electron source (via direct EU) and CO2 as a carbon source [40] Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 Electrochemically deposited Prussian blue (PB) complex enhanced the direct EU by 3.8 times [41] PCP poised cathode potential, SHE standard hydrogen electrode, EU electron uptake, DIET direct interspecies electron transfer, PHB polyhydroxybutyrate, NA not applicable Open in new tab Examples of direct microbial electron uptake (direct EU) by different electrotrophs for microbial electrosynthesis (MES) Microbial group . Electrotrophs . Application . PCP vs. SHE . Potential mechanism of EU/biological phenomenon noted . References . Acetogens Moorella thermoautotrophica, Moorella thermoacetica (thermophile) MES − 0.4 Temperature-dependent carbon dioxide (CO2) reduction to acetate via EU at 60 °C [15] Co-culture of Sporomusa ovata/Desulfobulbus propionicus MES NA Sulfide oxidation by D. propionicus. Electrons generated were then used by S. ovata to reduce CO2 to acetate on a graphite cathode [17] Sporomusa ovata MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate by S. ovata [33] Sporomusa silvacetica, Sporomusa sphaeroides, Clostridium ljungdahlii, Clostridium aceticum MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate [32] Methanogens Marine lithoautotrophic methanobacterium-like archaeon strain IM1 Electromethanogenesis − 0.4 Direct EU from graphite cathodes to convert CO2 to methane (CH4) without hydrogen serving as a cathode-generated electron carrier [2] Methabacterium palustre Electromethanogenesis − 1.0 Direct EU from the cathode to convert CO2 to CH4 [7] Methanococcus maripaludis (electromethanogenic archaeon) MES − 0.6 Surface-associated redox enzymes and formate dehydrogenases are involved in direct EU [30] Mixed methanogenic culture Electromethanogenesis − 1.5 Electrically reduced neutral red (NR) served as the sole source of reducing power for growth and metabolism of a mixed methanogenic culture in the MES system [34] Methanothermobacter thermautotrophicus Electromethanogenesis NA Applied voltage as a reducing power source to reduce CO2 to CH4 [45] Mixed methanogenic culture Electromethanogenesis − 0.456 Applied cathodic potential and environmental conditions are key factors for “electrometabolism” [46] Methanosaeta and Methanosarcina (acetoclastic methanogens) Electromethanogenesis − 0.7 Antibiotics pretreatment effectively inhibited hydrogen (H2)-utilizing methanogens and significantly promoted the growth of acetoclastic methanogens [54] Bioreactors enriched in Methanobacterium sp. methanogens Electromethanogenesis − 0.7 Multiple pathways of electron transfer, including direct cathode-to-cell, interspecies exchange, and semi-conductive conduits implicated [60] Photoautotrophic microbes Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 The pioABC operon that is essential for photoautotrophic growth by ferrous iron (Fe(II)) oxidation, influences direct electron uptake from the cathode [5] Green sulfur bacterium Prosthecochloris aestaurii with a heterotrophic partner bacterium Geobacter sulfurreducens No application explored (mechanistic study) − 0.401 Anoxygenic photosynthesis by P. aestaurii is driven by electrons derived either from a solid electrode or acetate oxidation via direct interspecies electron transfer (DIET) from G. sulfurreducens [18] Rhodopseudomonas palustris TIE-1 MES + 0.1 Intracellular accumulation of PHB with light as an energy source, poised electrodes as electron source (via direct EU) and CO2 as a carbon source [40] Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 Electrochemically deposited Prussian blue (PB) complex enhanced the direct EU by 3.8 times [41] Microbial group . Electrotrophs . Application . PCP vs. SHE . Potential mechanism of EU/biological phenomenon noted . References . Acetogens Moorella thermoautotrophica, Moorella thermoacetica (thermophile) MES − 0.4 Temperature-dependent carbon dioxide (CO2) reduction to acetate via EU at 60 °C [15] Co-culture of Sporomusa ovata/Desulfobulbus propionicus MES NA Sulfide oxidation by D. propionicus. Electrons generated were then used by S. ovata to reduce CO2 to acetate on a graphite cathode [17] Sporomusa ovata MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate by S. ovata [33] Sporomusa silvacetica, Sporomusa sphaeroides, Clostridium ljungdahlii, Clostridium aceticum MES − 0.4 Poised graphite electrode as a source of electrons for the reduction of CO2 to acetate [32] Methanogens Marine lithoautotrophic methanobacterium-like archaeon strain IM1 Electromethanogenesis − 0.4 Direct EU from graphite cathodes to convert CO2 to methane (CH4) without hydrogen serving as a cathode-generated electron carrier [2] Methabacterium palustre Electromethanogenesis − 1.0 Direct EU from the cathode to convert CO2 to CH4 [7] Methanococcus maripaludis (electromethanogenic archaeon) MES − 0.6 Surface-associated redox enzymes and formate dehydrogenases are involved in direct EU [30] Mixed methanogenic culture Electromethanogenesis − 1.5 Electrically reduced neutral red (NR) served as the sole source of reducing power for growth and metabolism of a mixed methanogenic culture in the MES system [34] Methanothermobacter thermautotrophicus Electromethanogenesis NA Applied voltage as a reducing power source to reduce CO2 to CH4 [45] Mixed methanogenic culture Electromethanogenesis − 0.456 Applied cathodic potential and environmental conditions are key factors for “electrometabolism” [46] Methanosaeta and Methanosarcina (acetoclastic methanogens) Electromethanogenesis − 0.7 Antibiotics pretreatment effectively inhibited hydrogen (H2)-utilizing methanogens and significantly promoted the growth of acetoclastic methanogens [54] Bioreactors enriched in Methanobacterium sp. methanogens Electromethanogenesis − 0.7 Multiple pathways of electron transfer, including direct cathode-to-cell, interspecies exchange, and semi-conductive conduits implicated [60] Photoautotrophic microbes Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 The pioABC operon that is essential for photoautotrophic growth by ferrous iron (Fe(II)) oxidation, influences direct electron uptake from the cathode [5] Green sulfur bacterium Prosthecochloris aestaurii with a heterotrophic partner bacterium Geobacter sulfurreducens No application explored (mechanistic study) − 0.401 Anoxygenic photosynthesis by P. aestaurii is driven by electrons derived either from a solid electrode or acetate oxidation via direct interspecies electron transfer (DIET) from G. sulfurreducens [18] Rhodopseudomonas palustris TIE-1 MES + 0.1 Intracellular accumulation of PHB with light as an energy source, poised electrodes as electron source (via direct EU) and CO2 as a carbon source [40] Rhodopseudomonas palustris TIE-1 No application explored (mechanistic study) + 0.1 Electrochemically deposited Prussian blue (PB) complex enhanced the direct EU by 3.8 times [41] PCP poised cathode potential, SHE standard hydrogen electrode, EU electron uptake, DIET direct interspecies electron transfer, PHB polyhydroxybutyrate, NA not applicable Open in new tab Microbial electrosynthesis (MES) leads to the recognition of EU MES is an extensively studied bioelectrochemical process that exploits electrotrophs to produce biofuels or bioelectrocommodities by reducing the greenhouse gas CO2 [3, 13, 42]. Because CO2 is a primary driver of global warming, this approach can be very promising for a future electricity-driven economy that leverages renewable energy sources for carbon neutral bioproduction. Other promising advantages of MES are that: (i) electrical power supplied to an MES cathode is directly proportional to the bioelectrocommodities produced [8, 58], (ii) MES allows sustainable and economical production of various chemicals (reactions 1–4) such as acetic acid (CH3COOH) [31], propionic acid (CH3CH2COOH) [31, 58], methanol (CH3OH) [55], and ethanol (CH3CH2OH) [4] using CO2 as substrate following the reactions (1–4) below. 2CO2+6H2O+8e-→CH3COOH+4H2O+2O2, $$2{\text{CO}}_{2} + 6{\text{H}}_{2} {\text{O }} + \, 8e^{ - } \to {\text{CH}}_{3} {\text{COOH }} + \, 4{\text{H}}_{2} {\text{O }} + 2{\text{O}}_{2} ,$$1 3CO2+10H2O+6e-→CH3CH2COOH+7H2O+3.5O2, $$3{\text{CO}}_{2} + \, 10{\text{H}}_{2} {\text{O }} + 6e^{ - } \to {\text{CH}}_{3} {\text{CH}}_{2} {\text{COOH }} + \, 7{\text{H}}_{2} {\text{O }} + 3.5{\text{O}}_{2} ,$$2 CO2+3H2O+6e-→CH3OH+H2O+1.5H2O, $${\text{CO}}_{2} + \, 3{\text{H}}_{2} {\text{O }} + \, 6e^{ - } \to {\text{CH}}_{3} {\text{OH }} + {\text{ H}}_{2} {\text{O }} + \, 1.5{\text{H}}_{2} {\text{O,}}$$3 2CO2+9H2O+18e-→CH3CH2OH+6H2O+3O2. $$2{\text{CO}}_{2} + \, 9{\text{H}}_{2} {\text{O }} + \, 18e^{ - } \to {\text{CH}}_{3} {\text{CH}}_{2} {\text{OH }} + \, 6{\text{H}}_{2} {\text{O }} + \, 3{\text{O}}_{2} .$$4 Furthermore, MES offers a new application for biorefineries that integrate biomass conversion processes and equipment to produce fuels, power, heat, and value-added chemicals. Despite these advantages, MESs also have some limitations, such as (i) CO2 (often used substrate in MES) is thermodynamically very stable and requires significant power from poised electrodes (cathode) to produce electron-rich bioelectrocommodities [9], and (ii) low electron transfer rates from cathodes to microbes can restrict the production of commercially feasible bioelectrocommodities [4, 12]. Although higher electron transfer rates from charged cathodes to microbes can be achieved at low cathode potentials [more negative potential compared to standard hydrogen electrode (SHE) potential], achieving such low potentials require high power supplies that eventually will reduce energetic efficiency [4, 28]. At these low cathodic potentials, inevitable electron-rich carriers, such as hydrogen (H2), are also produced electrochemically [11, 16, 30]. This can hinder the overall efficiency of electron conversion (electrons to products), eventually affecting the production cost of bioelectrocommodities. More importantly, effective production of bioelectrocommodities is limited by the lack of understanding of how microorganisms capture electrons from cathodes. Whereas mechanistic information about microbially catalyzed electron flow towards electrodes such as in MFCs is abundant, information about EU is limited, which negatively affects the ability to optimize MES systems for the efficient production of bioelectrocommodities [8]. Indirect EU in MES MES can use cathodic H2 as an electron donor to drive the synthesis of carbon-containing chemicals. This cathodically evolved H2 can support microbial growth and is referred to as indirect or H2-mediated MES [4, 21]. Additionally, the versatile range of products that can be formed when microbial metabolism is driven by H2 makes this approach a good stepping-stone towards the electricity-driven production of biochemicals [10, 38]. Experimental evidence suggests that poised cathode potentials (PCP) lower than − 0.590 V (PCP vs. SHE) are favorable for the abiotic evolution of H2. This electrochemically generated H2 can act as an electron donor for microbial metabolism coupled with CO2 reduction [4, 10, 21, 44]. This is exemplified in a comparative study of CO2 reduction at two different PCPs, − 0.360 V and − 0.660 V [4]. Using stainless steel as a cathode material produced higher amounts of acetate (244 ± 20 mg L−1) at − 0.660 V, and this was attributed to higher H2 evolution at this potential [4]. Although an excellent initial strategy, H2-mediated MES has some weaknesses such as (i) low solubility of H2; (ii) requirement of a pressurized environment to produce high concentrations of biochemicals; and (iii) more importantly, a higher electrical energy requirement resulting in reduced energetic efficiency. Thus, using low negative potentials to exclude the probability of the abiotic evolution of H2 at cathodes is recommended for the safe and efficient operation of MES reactors. In contrast, if the PCP is below − 1.5 V, formate is generated [20, 29]. Formate is highly soluble and is readily converted to CO2 and NADH in the cells, providing a safe replacement for H2 [29]. Electrochemically generated formate has been previously used to shuttle electrons from the cathode to Ralstonia eutropha H16 to produce isobutanol and 3-methyl-1-butanol ((CH3)2CHCH2CH2OH) [29]. However, employing such low cathode potentials requires more electrical energy, which eventually reduces the overall energetic efficiency of the MES system. Additional electron shuttles such as ammonia and Fe2+ can be beneficial because they require less electrical energy. But again, using these shuttles as electron mediators is not very efficient because of the low electron-transfer rates and significantly reduced conversion rates of CO2 to useful biochemicals. It has also been suggested that more complex biomolecules such as flavins and DNA can act as indirect electron mediators in BES systems. In some cases, soluble redox mediators (electron shuttles) are used to overcome H2 evolution at the cathode surface, including neutral red (NR), E0 = − 0.325 V [19], methyl viologen (MV), E0 = − 0.440 V [35, 49], anthraquinone-2,6-disulfonate (AQDS), E0 = − 0.184 V [50], and thionin, E0 = 0.060 V [49]. Although the use of soluble redox mediators is promising, their chemical instability, toxicity to microbes and difficulty in separating them from products [9] could potentially limit their applications as electron shuttles in MES systems. The direct supply of cathodic electrons to electrotrophs is more sustainable and energy efficient in bioelectronic applications due to the fact that these organisms require lower electrical energy to maintain their growth. Direct EU in MES Certain microbes can take up electrons directly (direct EU) from electrodes in the absence of added/self-produced mediators or electrochemically evolved chemicals [2]. In this case, higher PCPs are used to operate cathodes so that H2 or other mediators are not produced. Thus, direct EU is more promising and cost-effective for producing bioelectrocommodities using an external supply of electrical energy [33]. Direct EU from cathodes or electroconductive materials for MES has been implicated by certain groups of electrotrophic bacteria such as acetogens, methanogens, and photosynthetic iron oxidizers. Table 1 summarizes examples and potential mechanisms of direct EU for MES by these organisms. Direct EU by acetogens Acetogenic electrotrophs are capable of converting CO2 into acetate and other multi-carbon molecules via direct EU. The principle of electroacetogenesis was first shown for the acetogen, Sporomusa ovata, at PCP of − 0.400 V [33]. S. ovata used 85% of captured electrons for the conversion of CO2 into acetate and a small quantity of 2-oxobutyrate suggesting that microbiological catalysts may be a robust alternative when coupled with photovoltaics. Other pure cultures of acetogenic electrotrophs, such as S. silvacetica, S. sphaeroides, Clostridium ljungdahlii, Acetobacterium woodii, and C. aceticum have successfully been used to produce acetate at a PCP of − 0.400 V [33]. Acetate production was further improved by modifying the carbon cloth cathode with a material such as chitosan, cyanuric acid, 3-aminopropyltriethoxysilane, polyaniline, melamine, ammonia, Au-nanoparticles (Au-NPs), Pd-NPs, Ni-NPs, carbon nanotube (CNT)-cotton, and CNT-polyester [59]. These cathodic materials increased acetate production by ~ 80%. Interestingly, chitosan modified carbon cloth produced ~ 6 to 7 times higher acetate (229 mM m−2 day−1) compared to unmodified carbon cloth (30 mM m−2 day−1) with S. ovata as microbial catalyst at a PCP of − 0.400 V. This positive effect was due to enhanced bacterial attachment on the positively charged chitosan–carbon cathode surface [59]. The rate of acetate production by a previously established (operated over 150 days) mixed community biocathode increased at a PCP of − 0.590 V (4–17 mM day−1) from CO2 [31]. However, the use of mixed community complicates the separation process and reduces the electricity conversion efficiency to a specific multi-carbon compound. In an attempt to make an MES system energetically efficient, strategies to reduce electrical supply from a cathode to an electrotroph have been studied recently. In a dual organism MES system, Desulfobulbus propionicus oxidized sulfide to sulfate at the anode while S. ovata reduced CO2 to acetate (24.8 mM day−1 m−2) at the cathode [17]. Because sulfide is an electron rich molecule, this strategy requires less electrical energy. However, using sulfides or organic waste products as electron donors require an efficient catalyst to recover electrons for CO2 reduction [17]. Acetogenic thermophiles such as Moorella thermoacetica and M. thermoautotrophica were investigated at a PCP of − 0.300 V from 25 to 70 °C [15]. In this study, higher acetate production was observed from M. thermoautotrophica (11.6 ± 0.9 mM day−1 m−2 at 60 °C) than M. thermoacetica (6.9 ± 0.6 mM day−1 m−2). Furthermore, immobilizing M. thermoautotrophica with carbon nanoparticles increased acetate production to 58.2 mM day−1 m−2, concomitant with enhanced EU (63.47 mA m− 2 at 55 °C) at a PCP of − 0.400 V [57]. Although acetogens seem promising organisms for MES studies, the mechanisms of energy conservation and electron transfer between acetogens and cathodes need further investigation. Direct EU by methanogens Methanogens are capable of converting CO2 to methane (CH4) using H2 as an electron donor via methanogenesis. Methanogens can take up electrons directly or indirectly from poised cathodes to convert CO2 into CH4. Indirect electromethanogenesis was investigated for the first time using mixed methanogenic cultures with electrically reduced neutral red (NR) as an electron mediator at a PCP of − 1.500 V [34]. Experimental evidence indicated that the artificial electron carrier, NR, enabled electrons to indirectly enter the electron transport chain, leading to the generation of a proton motive force (PMF) for energy conservation. This also allowed the organism to grow and produce CH4 from CO2. This was later followed by the discovery of direct EU by the methanogen, Methanobacterium palustre from a cathode to convert CO2 into CH4 in a process called “direct” electromethanogenesis [7]. Furthermore, methanogens can engage in direct interspecies electron transfer (DIET) with other microbes including other methanogens [47]. For example, a mixture of hydrogenotrophic (Methanosarcina sp.) and acetoclastic methanogens (Methanosaeta sp.) can convert CO2 into CH4 via DIET [56]. In another study on direct EU, researchers used a hydrogenase mutant of Methanococcus maripaludis to exclude the possibility of H2 mediated EU. This study indicates that strain M. maripaludis MM1284, deleted for catabolic (fru, frc, hmd, vhu and vhc) and anabolic (ehb) hydrogenase encoding genes, can directly take up cathodic electrons at a PCP of − 0.600 V [30]. Similarly, Deutzmann et al. [12] investigated the EU characteristics of M. maripaludis in an MES system. They showed that free, surface-associated redox enzymes, such as hydrogenases and presumably formate dehydrogenases can mimic direct EU during Fe(0) corrosion and microbial electrosynthesis. The authors suggest that direct EU by methanogens might represent an ecologically important mechanism of biological electron transfer. Several other studies suggest that methanogens can produce CH4 by directly accepting electrons from charged surfaces [2, 27, 37, 45, 48, 60]. However, the molecular mechanisms of direct electromethanogenesis are still unclear and await future research. Direct EU by photoautotrophic microbes Photoautotrophic iron oxidizers such as, Rhodopseudomonas palustris TIE-1 can directly use poised electrodes as electron donors for photoautotrophic growth at cathodic potentials that avoid electrolytic H2 production [5, 41]. Bose et al. [5] using TIE-1 with an electrically poised cathode as an electron source and light as an energy source revealed that TIE-1 can perform direct EU at a PCP of + 0.100 V with a current uptake of up to − 1.5 μA cm−2. The cathodic current uptake by the same organism was also studied at a PCP of − 0.022 V [14]. In this study, Fe(III) was electrochemically reduced to Fe(II) in a separate abiotic reactor that was then supplied to the biotic reactor. In the biotic reactor, TIE-1 performed phototrophic iron oxidation to generate Fe(III), which was then returned to the abiotic reactor for its subsequent electrochemical reduction. This study, therefore, demonstrated indirect EU by TIE-1 using soluble iron as an electron mediator [14]. However, a recent study tested the ability of iron-based redox mediators to enhance direct EU by TIE-1 at a PCP of + 0.100 V. This study showed that soluble iron cannot be used as an electron mediator for indirect EU by TIE-1 at this PCP, and also that direct EU can be augmented using an insoluble iron matrix such as Prussian Blue complex [41]. The same group has further demonstrated that TIE-1 can produce polyhydroxybutyrate (PHB) while performing direct EU, showing that photoautotrophic iron oxidizers can be leveraged for MES [40]. An MES system using a co-culture of the photoautotrophic green sulfur bacterium, Prosthecochloris aestaurii, and a heterotrophic partner bacterium, Geobacter sulfurreducens demonstrated a direct link between anoxygenic photosynthesis and anaerobic respiration suggesting phototrophy [18]. Experimental evidence suggested that phototrophy can be driven by electrons derived either from a solid electrode at a PCP of − 0.401 V or acetate oxidation via DIET from a heterotrophic partner bacterium, Geobacter sulfurreducens. P. aestaurii growth was limited with a G. sulfurreducens mutant lacking a trans-outer membrane porin-cytochrome protein complex (OmbB–OmaB–OmcB–OrfS–OmbC–OmaC–OmcC) that is essential for electron transfer to electrodes/ferrihydrite [18]. This metabolism known as syntrophic anaerobic photosynthesis expands new possibilities for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities via direct photoelectrotrophy. Photoautotrophic microbes possess significant advantages over heterotrophic organisms for MES applications due to their ability to use light as an energy source to fix CO2. Summary and future perspectives Even though the ability of electrotrophs to take up electrons from conductive materials has been explored for producing bioelectrocommodities via MES, a detailed understanding of how electrons are transferred from the conductive materials to the microbial catalyst remains incomplete especially for those performing direct EU. As such, mechanistic information about microbially catalyzed electron flow from charged materials to electrotrophs needs to be understood to make MES an energetically efficient, environmentally friendly, and versatile production strategy. Future studies need to focus on understanding the mechanisms underpinning direct EU and leveraging this knowledge to devise better strategies for bioproduction via synthetic biology and metabolic engineering. Direct EU and its use in bioelectronics applications have not been explored. For such applications, direct EU-capable microbes might be most advantageous because of the lower electrical energy required to maintain their growth. Thus, lower electrical output systems such as MFCs or biophotovoltaics can be used to grow and maintain direct-EU capable microbes. Similar to exoelectrogens, microbes capable of carrying out direct EU may also offer many opportunities to produce sustainable and economic bioinspired materials, a promising future direction that needs further attention. To scale up and improve the efficiency of MES, hybrid type photo-assisted MES (bio-based conversion of solar energy to bioproducts) needs to be explored using low resistive electrolytes and reactor design, hydrogen evolution catalysts and engineered microbial catalysts. Acknowledgements The authors would like to acknowledge financial support from the U.S. Department of Energy (Grant number DESC0014613), the David and Lucile Packard Foundation (Grant number 201563111), and the U.S. Department of Defense, Army Research Office (Grant number W911NF-18-1-0037). We would also like to thank Marta Wegorzewska, Washington University in St. Louis, USA for feedback on the manuscript. Author contributions RK, RS, and AB performed a necessary literature search. RK, RS, and AB wrote the manuscript. AB and RS helped with critical reading and shaping of the manuscript. RK and RS contributed equally to this work. All authors reviewed and contributed to the final version of the manuscript. Compliance with ethical standards Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. References 1. 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TI - Microbial electron uptake in microbial electrosynthesis: a mini-review
JF - Journal of Industrial Microbiology and Biotechnology
DO - 10.1007/s10295-019-02166-6
DA - 2019-10-01
UR - https://www.deepdyve.com/lp/oxford-university-press/microbial-electron-uptake-in-microbial-electrosynthesis-a-mini-review-fLn7LieLdR
SP - 1419
EP - 1426
VL - 46
IS - 9-10
DP - DeepDyve
ER -