Electrochemical interaction of Shewanella oneidensis MR-1 and its outer membrane cytochromes OmcA and MtrC with hematite electrodes

Leisa A Meitl,Carrick M Eggleston,Patricia J.S Colberg,Nidhi Khare,Catherine L Reardon,Liang Shi

doi:10.1016/j.gca.2009.06.021

Leisa A Meitl, Carrick M Eggleston + Show 4 more

Open Access

https://doi.org/10.1016/j.gca.2009.06.021

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Abstract

Bacterial metal reduction is an important biogeochemical process in anaerobic environments. An understanding of electron transfer pathways from dissimilatory metal-reducing bacteria (DMRB) to solid phase metal (hydr)oxides is important for understanding metal redox cycling in soils and sediments, for utilizing DMRB in bioremedation, and for developing technologies such as microbial fuel cells. Here we hypothesize that the outer membrane cytochromes OmcA and MtrC from Shewanella oneidensis MR-1 are the only terminal reductases capable of direct electron transfer to a hematite working electrode. Cyclic voltammetry (CV) was used to study electron transfer between hematite electrodes and protein films, S. oneidensis MR-1 wild-type cell suspensions, and cytochrome deletion mutants. After controlling for hematite electrode dissolution at negative potential, the midpoint potentials of adsorbed OmcA and MtrC were measured (−201 mV and −163 mV vs. Ag/AgCl, respectively). Cell suspensions of wild-type MR-1, deletion mutants deficient in OmcA (Δ omcA), MtrC (Δ mtrC), and both OmcA and MtrC (Δ mtrC–Δ omcA) were also studied; voltammograms for Δ mtrC–Δ omcA were indistinguishable from the control. When the control was subtracted from the single deletion mutant voltammograms, redox peaks were consistent with the present cytochrome (i.e., Δ omcA consistent with MtrC and Δ mtrC consistent with OmcA). The results indicate that OmcA and MtrC are capable of direct electron exchange with hematite electrodes, consistent with a role as terminal reductases in the S. oneidensis MR-1 anaerobic respiratory pathway involving ferric minerals. There was no evidence for other terminal reductases operating under the conditions investigated. A Marcus-based approach to electron transfer kinetics indicated that the rate constant for electron transfer k et varies from 0.025 s −1 in the absence of a barrier to 63.5 s −1 with a 0.2 eV barrier.

Highlights

Bacterial metal reduction is a key biogeochemical process in anaerobic environments
We use voltammetry to study both the energetics and kinetics of electron transfer between hematite electrodes and Dissimilatory metal-reducing bacteria (DMRB) as well as key enzymes isolated from DMRB
The controls showed that the hematite electrodes can be reductively dissolved at the most negative potentials used in our experiments, leading to a release of redox-active iron that produces artifactual redox peaks not attributable to adsorbed protein or organisms

Summary

Introduction

The most common natural redox-active metals, Fe and Mn, are insoluble at mid-range pH, necessitating either a microbe-to-mineral respiratory electron transfer pathway or Fe(III) solubilization and reduction. Dissimilatory metal-reducing bacteria (DMRB) have been the focus of much recent work because of their abundance in a wide range of natural environments and their involvement in global redox cycling (Myers and Nealson, 1988; Lovley, 1991, 1993, 1997; Lovley et al, 1991; Venkateswaran et al, 1999). DMRB can use a wide variety of compounds as terminal electron acceptors, including organic compounds and redox sensitive metals and radionuclides such as oxidized forms of U, Tc, Np, Pu, V, Mo, Cr, and Se (e.g., Lloyd, 2003; Carpentier et al, 2005; Fredrickson et al, 2008).

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