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.
Abstract. Cable bacteria (CB) are multicellular, filamentous bacteria within the family of Desulfobulbaceae that transfer electrons longitudinally from cell to cell to couple sulfide oxidation and oxygen reduction in surficial aquatic sediments. In the present study, electrochemical reactors that contain natural sediments are introduced as a tool for investigating the growth of CB on electrodes poised at an oxidizing potential. Our experiments utilized sediments from Yaquina Bay, Oregon, USA, and we include new phylogenetic analyses of separated filaments to confirm that CB from this marine location cluster with the genus “Candidatus Electrothrix”. These CB may belong to a distinctive lineage, however, because their filaments contain smaller cells and a lower number of longitudinal ridges compared to cables described from other locales. The results of a 135 d bioelectrochemical reactor experiment confirmed that these CB can migrate out of reducing sediments and grow on oxidatively poised electrodes suspended in anaerobic seawater. CB filaments and several other morphologies of Desulfobulbaceae cells were observed by scanning electron microscopy and fluorescence in situ hybridization on electrode surfaces, albeit in low densities and often obscured by mineral precipitation. These findings provide new information to suggest what kinds of conditions will induce CB to perform electron donation to an electrode surface, further informing future experiments to culture CB outside of a sediment matrix.
Members in the family of Desulfobulbaceae may be influential in various anaerobic microbial communities, including those in anoxic aquatic sediments and water columns, and within wastewater treatment facilities and bioelectrochemical systems (BESs) such as microbial fuel cells (MFCs). However, the diversity and roles of the Desulfobulbaceae in these communities have received little attention, and large portions of this family remain uncultured. Here we expand on findings from an earlier study (Li, Reimers, and Alleau, 2020) to more fully characterize Desulfobulbaceae that became prevalent in biofilms on oxidative electrodes of bioelectrochemical reactors. After incubations, DNA extraction, microbial community analyses, and microscopic examination, we found that a group of uncultured Desulfobulbaceae were greatly enriched on electrode surfaces. These Desulfobulbaceae appeared to form filaments with morphological features ascribed to cable bacteria, but the majority were taxonomically distinct from recognized cable bacteria genera. Thus, the present study provides new information about a group of Desulfobulbaceae that can exhibit filamentous morphologies and respire on the oxidative electrodes. While the phylogeny of cable bacteria is still being defined and updated, further enriching these members can contribute to the overall understanding of cable bacteria and may also lead to identification of successful isolation strategies.
The scope of the present study is to introduce electrochemical reactors as a tool for investigating the growth of novel filamentous cable bacteria and their unique extracellular electron transfer ability. New evidence that cable bacteria are widely distributed in sediments throughout an estuarine system connected to the NE Pacific Ocean is also presented. Cable bacteria found within Yaquina Bay, Oregon, USA, appear to cluster with the genus, Candidatus Electrothrix. Results of a 135-day bioelectrochemical reactor experiment confirm a previous observation that cable 10 bacteria can grow on oxidatively poised electrodes suspended in anaerobic seawater above reducing sediments.However, several diverse morphologies of Desulfobulbaceae filaments, cells, and colonies were observed on the carbon fibers of the suspended electrodes including encrusted chains of cells. These observations provide new information to suggest what conditions will induce cable bacteria to perform electron donation to an electrode surface, further informing future experiments to culture cable bacteria apart from a sediment matrix. 15 IntroductionLong distance electron transfer (LDET) is a mechanism used by certain microorganisms to generate energy through the transfer of electrons over distances greater than a cell-length. These microorganisms may pass electrons across dissolved redox shuttles, nanofiber-like cell appendages, outer-membrane cytochromes, and/or mineral nanoparticles to connect extracellular electron donors and acceptors Lovley, 2016). Recently, a novel type of LDET 20 exhibited by filamentous bacteria in the family of Desulfobulbaceae was discovered in the uppermost centimeters of various aquatic, but mainly marine, sediments (Malkin et al., 2014;Pfeffer et al., 2012). These filamentous bacteria, also known as "cable bacteria", electrically connect two spatially separated redox half-reactions and generate electrical current over distances that can extend to centimeters, which is an order of magnitude longer than previously recognized LDET distances (Meysman, 2017). 25The unique ability of cable bacteria to perform LDET creates a spatial separation of oxygen reduction in oxic surface layers of sediment from sulfide oxidation in subsurface layers (Meysman, 2017). The spatial separation of these two half-reactions also creates localized porewater pH extremes in oxic and sulfidic layers, which induces a series of secondary reactions that stimulate the geochemical cycling of elements such as iron, manganese, calcium, phosphorus, and nitrogen (Kessler et al., 2018;Rao et al., 2016; Seitaj et al., 2015;Sulu-Gambari et al., 2016b, 2016a. In addition 30 to altering established perceptions of sedimentary biogeochemical cycling and microbial ecology (Meysman, 2017;Nielsen and Risgaard-Petersen, 2015), cable bacteria also possess intriguing structural features that may inspire new engineering applications in areas of bioenergy harvesting and biomaterial design (Lovley, 2016). Pfeffer et al., 2012). Therefore to initiate this enquiry, sedimen...
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