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Microbial Electron Uptake in Microbial Electrosynthesis: a Mini-Review

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Microbial Electron Uptake in Microbial Electrosynthesis: a Mini-Review Journal of Industrial Microbiology & Biotechnology (2019) 46:1419–1426 https://doi.org/10.1007/s10295-019-02166-6 BIOENERGY/BIOFUELS/BIOCHEMICALS - MINI REVIEW Microbial electron uptake in microbial electrosynthesis: a mini‑review Rengasamy Karthikeyan1 · Rajesh Singh1 · Arpita Bose1 Received: 13 December 2018 / Accepted: 23 March 2019 / Published online: 28 March 2019 © Society for Industrial Microbiology and Biotechnology 2019 Downloaded from https://academic.oup.com/jimb/article/46/9-10/1419/6017417 by guest on 24 September 2021 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 bioelec- trochemical 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 efcient. 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. Keywords Microbial electrosynthesis · Bioelectrochemical system · Microbial electron uptake · Direct EU · Indirect EU Introduction often called exoelectrogens. This microbial ability has been utilized for various applications, such as bioremediation, Oxidation–reduction reactions are responsible for energy energy generation and biosynthesis [23, 25, 36]. But MECs transformations by nearly all life-forms. Most organisms are perhaps equally, if not more important, for scaled appli- use soluble oxidants and reductants as electron-acceptors or cations. They also use a bioanode and rely on small energy -donors. Some microorganisms can, however, acquire energy input to set a diferential voltage and make H 2 at the cathode through electron transfer to or from extracellular solid inor- [1, 6]. In contrast, MES is a biocathode-driven approach, ganic compounds, using them as electron-acceptors or and it is a recently described bioelectrochemical process that -donors, respectively. This microbial metabolism is specif- uses microbes to produce biofuels or bioelectrocommodi- cally termed as “extracellular electron transfer (EET)” [22, ties from carbon dioxide (CO2) and electricity. It involves 24, 53]. EET is a widespread process in nature and is critical EET from an electrode/cathode (or from solid conductive for biogeochemical cycling of various elements. In addition, materials such as iron minerals) to microbes [5, 39, 51]. EET has also been leveraged for a number of applications. This form of EET is also called microbial electron uptake EET plays an important role in bioelectrochemical sys- (abbreviate this as EU throughout). EU-capable microbes tems and associated applications. These applications can be are called “electrotrophs” and can consume electricity from categorized mainly into (i) microbial fuel cells (MFC), (ii) electrodes or electrons from electroconductive solid materi- microbial electrolysis cells (MEC), and (iii) microbial elec- als to produce value-added multi-carbon products [43, 58]. trosynthesis (MES). MFCs are bioanode-driven systems, and Various studies have shown that MES can occur via either they produce electricity by wiring a bioanode to a chemical indirect or direct EU. In direct EU, microorganisms attach to cathodic reaction (O2 or ferricyanide) [23]. It involves EET solid electroconductive surfaces (cathodes or iron minerals) from microbes to an electrode/anode. These microbes are 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 * Arpita Bose difusible chemicals that are either produced electrochemi- [email protected] cally or added to the reactors [14, 19, 26, 29, 35, 47, 49, 52] 1 Department of Biology, Washington University in Saint (Fig. 1). Louis, One Brookings Drive, St. Louis, MO 63130, USA Vol.:(0123456789)1 3 1420 Journal of Industrial Microbiology & Biotechnology (2019) 46:1419–1426 Fig. 1 a Schematic of extra- cellular electron uptake (EU) pathways adopted in microbial electrosynthesis (MES) at dif- ferent poised cathode potentials (PCP) vs. standard hydrogen electrode (SHE). (Mox mediator oxidation, Mrd mediator reduc- tion, PHB polyhydroxybutyrate) Downloaded from https://academic.oup.com/jimb/article/46/9-10/1419/6017417 by guest on 24 September 2021 The primary focus of this mini-review is to discuss the ethanol (CH3CH2OH) [4] using CO2 as substrate following recent advances and challenges of direct EU from solid the reactions (1–4) below. poised electrodes in MES as it is less well-studied than indi- − 2CO2 + 6H2O + 8e → CH3COOH + 4H2O + 2O2, rect EU. This mini-review provides examples where direct (1) EU has been implicated for MES (Table 1). In addition, this e− → mini-review is intended to highlight the fact that applica- 3CO2 + 10H2O + 6 CH3CH2COOH + 7H2O + 3.5O2, tions and mechanistic studies go hand-in-hand when study- (2) ing microbe-charged surface interactions. CO + 3H O + 6e− → CH OH + H O + 1.5H O, 2 2 3 2 2 (3) 2CO + 9H O + 18e− → CH CH OH + 6H O + 3O . Microbial electrosynthesis (MES) leads 2 2 3 2 2 2 to the recognition of EU (4) Furthermore, MES ofers a new application for biore- fneries that integrate biomass conversion processes and MES is an extensively studied bioelectrochemical process equipment to produce fuels, power, heat, and value-added that exploits electrotrophs to produce biofuels or bioelec- chemicals. Despite these advantages, MESs also have some trocommodities by reducing the greenhouse gas CO [3, 13, 2 limitations, such as (i) CO (often used substrate in MES) 42]. Because CO is a primary driver of global warming, 2 2 is thermodynamically very stable and requires signifcant this approach can be very promising for a future electricity- power from poised electrodes (cathode) to produce electron- driven economy that leverages renewable energy sources for rich bioelectrocommodities [9], and (ii) low electron transfer carbon neutral bioproduction. Other promising advantages rates from cathodes to microbes can restrict the production of MES are that: (i) electrical power supplied to an MES of commercially feasible bioelectrocommodities [4, 12]. cathode is directly proportional to the bioelectrocommodi- Although higher electron transfer rates from charged cath- ties produced [8, 58], (ii) MES allows sustainable and eco- odes to microbes can be achieved at low cathode potentials nomical production of various chemicals (reactions 1–4) [more negative potential compared to standard hydrogen such as acetic acid (CH COOH) [31], propionic acid 3 electrode (SHE) potential], achieving such low potentials (CH3CH2COOH) [31, 58], methanol (CH3OH) [55], and 1 3 Journal of Industrial Microbiology & Biotechnology (2019)46:1419–1426 Journal ofIndustrial Microbiology &Biotechnology Table 1 Examples of direct microbial electron uptake (direct EU) by diferent electrotrophs for microbial electrosynthesis (MES) Microbial group Electrotrophs Application PCP vs. SHE Potential mechanism of EU/biological References phenomenon noted Acetogens Moorella thermoautotrophica, Moorella MES − 0.4 Temperature-dependent carbon dioxide [15] thermoacetica (thermophile) (CO2) reduction to acetate via EU at 60 °C Co-culture of Sporomusa ovata/Desulfobul- MES NA Sulfde oxidation by D. propionicus. [17] bus propionicus Electrons generated were then used by S. ovata to reduce CO2 to acetate on a graphite cathode Sporomusa ovata MES − 0.4 Poised graphite electrode as a source of [33] electrons for the reduction of CO2 to acetate by S. ovata Sporomusa silvacetica, Sporomusa MES − 0.4 Poised graphite electrode as a source of [32] sphaeroides, Clostridium ljungdahlii, electrons for the reduction of CO2 to Clostridium aceticum acetate Methanogens Marine lithoautotrophic methanobacterium- Electromethanogenesis − 0.4 Direct EU from graphite cathodes to [2] like archaeon strain IM1 convert CO2 to methane (CH4) without hydrogen serving as a cathode-generated electron carrier Methabacterium palustre Electromethanogenesis − 1.0 Direct EU from the cathode to convert CO2 [7] to CH4 Methanococcus maripaludis (electrometha- MES − 0.6 Surface-associated redox enzymes and [30] nogenic archaeon) formate dehydrogenases are involved in direct EU Mixed methanogenic culture Electromethanogenesis − 1.5 Electrically reduced neutral red (NR) [34] served as the sole source of reducing power for growth and metabolism of a mixed methanogenic culture in the MES system Methanothermobacter thermautotrophicus Electromethanogenesis NA Applied voltage as a reducing power source [45] to reduce CO2 to CH4 Mixed methanogenic culture Electromethanogenesis − 0.456 Applied cathodic potential and environ- [46] mental conditions are key factors for “electrometabolism” Methanosaeta and Methanosarcina (aceto- Electromethanogenesis − 0.7 Antibiotics pretreatment efectively inhib- [54] clastic methanogens) ited hydrogen (H2)-utilizing methanogens and signifcantly promoted
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