Abstract

Multicellular, filamentous, sulfur-oxidizing bacteria, known as cable bacteria, were discovered attached to fibers of a carbon brush electrode serving as an anode of a benthic microbial fuel cell (BMFC). The BMFC had been operated in a temperate estuarine environment for over a year before collecting anode samples for scanning electron microscopy and phylogenetic analyses. Individual filaments were attached by single terminus cells with networks of pilus-like nano-filaments radiating out from these cells, across the anode fiber surface, and between adjacent attachment locations. Current harvesting by the BMFC poised the anode at potentials of ~170–250 mV vs. SHE, and these surface potentials appear to have allowed the cable bacteria to use the anode as an electron acceptor in a completely anaerobic environment. A combination of catalyzed reporter deposition fluorescent in situ hybridization (CARD-FISH) and 16S rRNA gene sequence analysis confirmed the phylogeny of the cable bacteria and showed that filaments often occurred in bundles and in close association with members of the genera Desulfuromonas. However, the Desulfobulbaceae Operational Taxonomic Units (OTUs) from the 16S sequencing did not cluster closely with other putative cable bacteria sequences suggesting that the taxonomic delineation of cable bacteria is far from complete.

Highlights

  • Investigations of mechanisms that divert electrons from microbial catabolic activity to generate electricity between electrodes of a microbial fuel cell (MFC) have been instrumental in recent discoveries of new respiratory reactions, microbial syntrophy, and the conductive properties of biofilms (Schröder, 2007; Nevin et al, 2009; Lovley, 2012, 2017; Malvankar et al, 2012, 2014; Li et al, 2016)

  • To understand the conditions that led to the attachment of filamentous cable bacteria to carbon fiber anodes in the marine environment, we focus first on the cell potentials and current drawn from the benthic microbial fuel cell (BMFC) anode over the last 75 days of the deployment (Figure 3)

  • Models of electrogenic sulfur oxidation by cable bacteria have suggested that access to dissolved O2 or at least NO−3 was required for the maintainance of their overall metabolic activity (Marzocchi et al, 2014; Meysman et al, 2015; Matturro et al, 2017)

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Summary

Introduction

Investigations of mechanisms that divert electrons from microbial catabolic activity to generate electricity between electrodes of a microbial fuel cell (MFC) have been instrumental in recent discoveries of new respiratory reactions, microbial syntrophy, and the conductive properties of biofilms (Schröder, 2007; Nevin et al, 2009; Lovley, 2012, 2017; Malvankar et al, 2012, 2014; Li et al, 2016). There is a diversity of microorganisms known to employ various means of extracellular electron transfer such as constructing electrically conductive pili, Electrode-Attached Cable Bacteria producing outer membrane c-type cytochromes, excreting redox shuttling compounds that bind to surfaces, and connecting through conductive abiotic materials (Gorby et al, 2006; Marsili et al, 2008; Summers et al, 2010; Kato et al, 2012; Lovley, 2012). The most intensively studied are Geobacter and Shewanella species, many strains of which originate from the marine environment or riverine sediments, where they commonly reduce iron and manganese (oxyhydr)oxide minerals or elemental sulfur (S◦) (Lovley et al, 2011; Pirbadian et al, 2014). Significant quantities of the dissolved sulfide react chemically with iron (oxydr)oxides to form FeS, S◦, and FeS2, while a fraction is typically reoxidized after transport by diffusion or bioturbation to overlying oxic zones (Jørgensen and Kasten, 2006)

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