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Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium Ardenticatena maritima 110S.

ABSTRACT: Ardenticatena maritima strain 110S is a filamentous bacterium isolated from an iron-rich coastal hydrothermal field, and it is a unique isolate capable of dissimilatory iron or nitrate reduction among the members of the bacterial phylum Chloroflexi. Here, we report the ability of A. maritima strain 110S to utilize electrodes as a sole electron acceptor and donor when coupled with the oxidation of organic compounds and nitrate reduction, respectively. In addition, multicellular filaments with hundreds of cells arranged end-to-end increased the extracellular electron transfer (EET) ability to electrodes by organizing filaments into bundled structures, with the aid of microbially reduced iron oxide minerals on the cell surface of strain 110S. Based on these findings, together with the attempt to detect surface-localized cytochromes in the genome sequence and the demonstration of redox-dependent staining and immunostaining of the cell surface, we propose a model of bidirectional electron transport by A. maritima strain 110S, in which surface-localized multiheme cytochromes and surface-associated iron minerals serve as a conduit of bidirectional EET in multicellular filaments.

SUBMITTER: Kawaichi S

PROVIDER: S-EPMC5808234 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium Ardenticatena maritima 110S.

Kawaichi Satoshi S Yamada Tetsuya T Umezawa Akio A McGlynn Shawn E SE Suzuki Takehiro T Dohmae Naoshi N Yoshida Takashi T Sako Yoshihiko Y Matsushita Nobuhiro N Hashimoto Kazuhito K Nakamura Ryuhei R

Frontiers in microbiology 20180206

Ardenticatena maritima strain 110S is a filamentous bacterium isolated from an iron-rich coastal hydrothermal field, and it is a unique isolate capable of dissimilatory iron or nitrate reduction among the members of the bacterial phylum Chloroflexi. Here, we report the ability of A. maritima strain 110S to utilize electrodes as a sole electron acceptor and donor when coupled with the oxidation of organic compounds and nitrate reduction, respectively. In addition, multicellul ...[more]

PMID: 29467724

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Project description: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.

Project description:UnlabelledShewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneidensis. To determine the contribution of flavin electron shuttles in extracellular electron transfer, a transposon mutagenesis screen was performed with S. oneidensis to identify mutants unable to secrete flavins. A multidrug and toxin efflux transporter encoded by SO_0702 was identified and renamed bfe (bacterial flavin adenine dinucleotide [FAD] exporter) based on phenotypic characterization. Deletion of bfe resulted in a severe decrease in extracellular flavins, while overexpression of bfe increased the concentration of extracellular flavins. Strains lacking bfe had no defect in reduction of soluble Fe(III), but these strains were deficient in the rate of insoluble Fe(III) oxide reduction, which was alleviated by the addition of exogenous flavins. To test a different insoluble electron acceptor, graphite electrode bioreactors were set up to measure current produced by wild-type S. oneidensis and the ?bfe mutant. With the same concentration of supplemented flavins, the two strains produced similar amounts of current. However, when exogenous flavins were not supplemented to bioreactors, bfe mutant strains produced significantly less current than the wild type. We have demonstrated that flavin electron shuttling accounts for ~75% of extracellular electron transfer to insoluble substrates by S. oneidensis and have identified the first FAD transporter in bacteria.ImportanceExtracellular electron transfer by microbes is critical for the geochemical cycling of metals, bioremediation, and biocatalysis using electrodes. A controversy in the field was addressed by demonstrating that flavin electron shuttling, not direct electron transfer or nanowires, is the primary mechanism of extracellular electron transfer employed by the bacterium Shewanella oneidensis. We have identified a flavin adenine dinucleotide transporter conserved in all sequenced Shewanella species that facilitates export of flavin electron shuttles in S. oneidensis. Analysis of a strain that is unable to secrete flavins demonstrated that electron shuttling accounts for ~75% of the insoluble extracellular electron transfer capacity in S. oneidensis.

Dataset Information

Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium Ardenticatena maritima 110S.

Publications

Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium <i>Ardenticatena maritima</i> 110S.

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