Abstract
Electron exchange reactions between microbial cells and solid materials, referred to as extracellular electron transfer (EET), have attracted attention in the fields of microbial physiology, microbial ecology, and biotechnology. Studies of model species of iron-reducing, or equivalently, current-generating bacteria such as Geobacter spp. and Shewanella spp. have revealed that redox-active proteins, especially outer membrane c-type cytochromes (OMCs), play a pivotal role in the EET process. Recent (meta)genomic analyses have revealed that diverse microorganisms that have not been demonstrated to have EET ability also harbor OMC-like proteins, indicating that EET via OMCs could be more widely preserved in microorganisms than originally thought. A methanotrophic bacterium Methylococcus capsulatus (Bath) was reported to harbor multiple OMC genes whose expression is elevated by Cu starvation. However, the physiological role of these genes is unknown. Therefore, in this study, we explored whether M. capsulatus (Bath) displays EET abilities via OMCs. In electrochemical analysis, M. capsulatus (Bath) generated anodic current only when electron donors such as formate were available, and could reduce insoluble iron oxides in the presence of electron donor compounds. Furthermore, the current-generating and iron-reducing activities of M. capsulatus (Bath) cells that were cultured in a Cu-deficient medium, which promotes high levels of OMC expression, were higher than those cultured in a Cu-supplemented medium. Anodic current production by the Cu-deficient cells was significantly suppressed by disruption of MCA0421, a highly expressed OMC gene, and by treatment with carbon monoxide (CO) gas (an inhibitor of c-type cytochromes). Our results provide evidence of EET in M. capsulatus (Bath) and demonstrate the pivotal role of OMCs in this process. This study raises the possibility that EET to solid compounds is a novel survival strategy of methanotrophic bacteria.
Highlights
Extracellular electron transfer (EET) is the process by which some microorganisms exchange intracellular electrons with an extracellular electron donor/acceptor, including naturally occurring metal compounds and artificial electrodes, across the cell membrane (Lovley, 2008; Kato, 2015)
Considering that there has been no report that outer membrane c-type cytochromes (OMCs) are used for metabolic reactions other than EET, we can assume that EET via OMCs could be more widely conserved in microorganisms than originally thought
Some of the OMC genes form a gene cluster with a gene homologous to the β-barrel outer membrane protein of S. oneidensis, which has been observed to complex with OMCs in the outer membrane (Larsen and Karlsen, 2016). We considered it likely that M. capsulatus (Bath) possesses EET capability via OMCs; no experimental evidence has been provided for the existence of EET capability in methanotrophs, and the physiological functions of their OMCs have not been clarified
Summary
Extracellular electron transfer (EET) is the process by which some microorganisms exchange intracellular electrons with an extracellular electron donor/acceptor, including naturally occurring metal compounds and artificial electrodes, across the cell membrane (Lovley, 2008; Kato, 2015). The EET ability of M. capsulatus (Bath) was verified by assessing current-producing and Fe(III)reducing activities of cells cultured in the presence or absence of Cu. The contribution of OMCs to the EET ability was verified by investigating the effects of deletion of an OMC gene and supplementation of carbon monoxide (CO) (an inhibitor of cytochromes) on current-producing activities.
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