Microbial Extracellular Electron Transfer and Its Relevance to Iron Corrosion

bs_bs_banner Minireview Microbial extracellular electron transfer and its relevance to iron corrosion Souichiro Kato1,2,3* acetogenic bacteria and nitrate-reducing bacteria. 1Bioproduction Research Institute, National Institute of Abilities of EET and EMIC are now regarded as micro- Advanced Industrial Science and Technology (AIST), bial traits more widespread among diverse microbial 2-17-2-1 Tsukisamu-Higashi, Toyohira-ku, Sapporo, clades than was thought previously. In this review, Hokkaido 062-8517,Japan. basic understandings of microbial EET and recent 2Research Center for Advanced Science and progresses in the EMIC research are introduced. Technology, The University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo 153-8904, Japan. 3Division of Applied Bioscience, Graduate School of Introduction Agriculture, Hokkaido University, Kita-9 Nishi-9,Kita-ku, Acquisition of energy is an indispensable activity for all Sapporo, Hokkaido 060-8589, Japan. living organisms. Most organisms, including human beings, conserve energy through respiration, with Summary organic compounds and oxygen gas as the electron donor and acceptor respectively. In contrast, many Extracellular electron transfer (EET) is a microbial microorganisms have the ability to utilize diverse inor- metabolism that enables efficient electron transfer ganic compounds as the substrates for respiration. Fur- between microbial cells and extracellular solid materi- thermore, some particular microorganisms have the als. Microorganisms harbouring EET abilities have ability to acquire energy through transferring electrons to received considerable attention for their various or from extracellular solid compounds. This microbial biotechnological applications, including bioleaching metabolism is specifically termed as ‘extracellular elec- and bioelectrochemical systems. On the other hand, tron transfer (EET)’ (Gralnick and Newman, 2007; Rich- recent research revealed that microbial EET poten- ter et al., 2012). In addition to naturally occurring metal tially induces corrosion of iron structures. It has been minerals, microorganisms harbouring EET abilities can well known that corrosion of iron occurring under utilize artificial conductive materials, including graphite anoxic conditions is mostly caused by microbial and metal electrodes, as the electron donor or acceptor activities, which is termed as microbiologically influ- (Bond and Lovley, 2003; Gregory et al., 2004). This enced corrosion (MIC). Among diverse MIC mecha- microbial activity has received considerable attention for nisms, microbial EET activity that enhances biotechnological applications, including bioremediation of corrosion via direct uptake of electrons from metallic toxic metals and diverse bioelectrochemical systems iron, specifically termed as electrical MIC (EMIC), has (Arends and Verstraete, 2012; Logan and Rabaey, 2012; been regarded as one of the major causative factors. Kato, 2015). Besides, recent studies have disclosed that The EMIC-inducing microorganisms initially identified some microorganisms utilize zero-valent metallic iron as were certain sulfate-reducing bacteria and methano- their electron donor via EET metabolisms, which stimu- genic archaea isolated from marine environments. lates iron corrosion under anoxic conditions. This review Subsequently, abilities to induce EMIC were also introduces the basic knowledge in microbial EET meta- demonstrated in diverse anaerobic microorganisms bolisms and the recent research progresses on the rele- in freshwater environments and oil fields, including vance of microbial EET to iron corrosion. Received 28 July, 2015; revised 18 November, 2015; accepted 19 November, 2015. For correspondence. E-mail [email protected]; Microbial EET Tel. (+81) 11 857 8968; Fax (+81) 11 857 8915. Microbial Biotechnology (2016) 9(2), 141–148 As for commonly characterized energy metabolisms, doi:10.1111/1751-7915.12340 microorganisms first must incorporate substrates for Funding Information respiration into their cells, where oxidation and reduc- No funding information provided. ª 2016 The Author. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 142 S. Kato Fig. 1. The schematic images of three microbial EET mechanisms. A. Direct EET via outer membrane redox proteins. B. Direct EET via solid conductive matrix (e.g. conductive pili). C. Indirect EET via an electron mediator compound (Mred/Mox). tion of substrates proceed. In contrast, special molecu- et al., 2004; Marsili et al., 2008). Naturally occurring lar mechanisms are required for EET-based energy (e.g. humic substances) and artificial (e.g. quinone metabolisms, since microorganisms cannot incorporate derivatives, ferrocene derivatives) redox chemicals can solid materials into their cells. Mechanisms of microbial also work as electron mediators to propel microbial EET EET can be categorized into either direct or indirect (Jiang and Kappler, 2008; Watanabe et al., 2009; Nishio manners. In the direct EET, microorganisms attach to et al., 2013). The reader is referred to several excellent solid surfaces, to or from which they directly transfer review articles on the mechanisms of direct and indirect electrons (Fig. 1A). The molecular mechanisms for the EET (Hernandez and Newman, 2001; Shi et al., 2007; direct EET have been intensively investigated for some Lovley, 2008; Thrash and Coates, 2008; Watanabe iron-reducing and iron-oxidizing bacteria, including et al., 2009; Richter et al., 2012). Geobacter sulfurreducens, Shewanella oneidensis and Acidithiobacillus ferrooxidans (Stams et al., 2006; Microorganisms and corrosion of iron Weber et al., 2006; Shi et al., 2007; Castelle et al., 2008). These microorganisms utilize metal-containing Corrosion of iron is an electrochemical process consist- redox proteins, such as c-type cytochromes and rusti- ing of oxidation of metallic iron to ferrous ion (anodic cyanin, to electrically connect intracellular respiratory reaction, Eq. 1) and reduction of electron acceptor com- chains and extracellular solid materials. Furthermore, pounds (cathodic reaction): G. sulfurreducens and S. oneidensis were reported to 2þ þ À $ ð Þ; 0 ¼ : ; Fe 2e Fe 0 E0 0 47 V (1) produce conductive filamentous apparatus (pili and outer membrane extensions, respectively) that are where À0.47 V references the standard hydrogen elec- specifically termed as ‘nanowires’ (Reguera et al., trode (the same applies hereafter). In oxic environments, 2005; Gorby et al., 2006; Pirbadian et al., 2014). These the cathodic reaction is reduction of oxygen (Eq. 2) and microorganisms have the ability to transfer electrons to corrosion rate is relatively high (Fig. 2A): or from distantly located solid materials using the fila- þ À þ $ À; 0 ¼þ : : O2 4e 2H2O 4OH E0 0 82 V (2) ments as ‘electric wire’ (Fig. 1B). In contrast, some microorganisms indirectly transfer In contrast, the most common electron consuming reac- electrons to or from solid compounds using diffusible tion under anoxic condition is proton reduction to hydro- redox chemicals, referred to as electron mediators gen gas (Eq. 3) (Fig. 2B): (Watanabe et al., 2009). Microorganisms reduce (or oxi- þ À 0 2H þ 2e $ H2; E ¼0:41 V: (3) dize) intracellular electron mediators, after which the 0 reduced (or oxidized) electron mediators diffuse out of Theoretically, iron corrosion in anoxic environments does the cell to solid surfaces and donate (or accept) elec- not become a serious problem, since the proton reduc- trons, and then the oxidized (or reduced) mediators tion reaction on iron surfaces is usually a particularly return back into the cells and are again utilized as respi- slow reaction. However, iron corrosion under anoxic con- ratory substrates (Fig. 1C). Some microorganisms have ditions has often been reported, and in most cases it is the ability to synthesize low-molecular-weight organic thought to be mediated by microbial metabolic activities compounds that work as electron mediators, including (Lee et al., 1995; Hamilton, 2003; Beech and Sunner, phenazine compounds and flavin derivatives (Rabaey 2004; Videla and Herrera, 2005). ª 2016 The Author. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology, Microbial Biotechnology, 9, 141–148 Extracellular electron transfer and biocorrosion 143 Fig. 2. The schematic images of the iron corrosion mechanisms. Spontaneous, oxidative dissolution of metallic iron into ferrous iron (the anodic reaction) is the first step of corrosion in all of the cases. A. Under oxic conditions, electrons derived from iron oxidation are consumed by reduction of O2 (the cathodic reaction). + B. Under anoxic conditions, the possible cathodic reaction is the reduction of H into H2, while the corrosion rate is quite low. C. CMIC‐inducing SRB reduce sulfate into corrosive H2S, which stimulate the cathodic reaction and hence iron corrosion. In this case, SRB requires exogenous electron donors (ED, such as lactate and H2) to reduce sulfate and acquire energy. D. EMIC‐inducing microorganisms directly utilize electrons in metallic iron as the electron donor to stimulate iron corrosion. Sulfate reduction, methanogenesis, acetogenesis and nitrate reduction were reported as the electron‐accepting reactions (EAred/EAox). Corrosion of iron caused by microbial metabolism is recent studies

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