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.
Highlights
Redox gradients are generated by a variety of mechanisms in natural environments, and the electrical potential from these gradients can generate electric current, termed geoelectric current, when two such gradients are spatially segregated and electrically connected by a conduit
We investigated the electron transfer (EET) ability and the existence of surface-associated multiheme cytochromes of intact filaments of a pure-cultured filamentous bacterium
We provided evidence that A. maritima strain 110S has the ability to generate anodic and cathodic current when coupled with the oxidation of organic compounds and nitrate reduction, respectively (Figure 2)
Summary
Redox gradients are generated by a variety of mechanisms in natural environments, and the electrical potential from these gradients can generate electric current, termed geoelectric current, when two such gradients are spatially segregated and electrically connected by a conduit. Sediment dwelling uncultured multicellular filamentous bacteria of the family Desulfobulbaceae have been suggested to couple sulfide oxidation with oxygen or nitrate reduction over microbially large (>1 cm) distances (Nielsen et al, 2010; Pfeffer et al, 2012; Risgaard-Petersen et al, 2012; Schauer et al, 2014; Marzocchi et al, 2014; Larsen et al, 2015; Seitaj et al, 2015; Vasquez-Cardenas et al, 2015; RisgaardPetersen et al, 2015; Sulu-Gambari et al, 2016; Burdorf et al, 2017) Such long-range redox coupling reactions seem to require metabolic synchronization and perhaps metabolic specialization amongst cells within the same filament, since cells on each terminus of the filament could experience very different environments from each other. The hypothesis has been challenged by the direct measurement of centimeterlong electron transport through reduced marine sediments: they demonstrated electrical conductivities sufficient for the estimated electron fluxes without any filamentous microbes (Malvankar et al, 2015a,b)
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