Abstract

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.

Highlights

  • Long-distance electron transfer (LDET) is a mechanism used by certain microorganisms to generate energy through the transfer of electrons over distances greater than a celllength

  • A novel type of LDET 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; Trojan et al, 2016)

  • These filamentous bacteria, known as “cable bacteria” (CB), 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)

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Summary

Introduction

Long-distance electron transfer (LDET) is a mechanism used by certain microorganisms to generate energy through the transfer of electrons over distances greater than a celllength. Li et al.: Inducing the attachment of cable bacteria on oxidizing electrodes gitudinal ridges of CB filaments via electron hopping promoted by extracellular cytochromes positioned within a redox gradient or via conductive electronic structures such as pili (Bjerg et al, 2018; Cornelissen et al, 2018; Kjeldsen et al, 2019; Meysman et al, 2019; Pfeffer et al, 2012) These hypotheses await further verification, and CB remain uncultured and difficult to grow outside of sediment. In a previous benthic microbial fuel cell (BMFC) experiment in a marine estuary (Reimers et al, 2017), we serendipitously observed the attachment of CB to carbon fibers serving as an anode in an anaerobic environment above sediments This finding suggested that CB possess the ability to donate electrons to solid electron acceptors, and it indicated a range of cathodic potentials favorable for electron transfer (Reimers et al, 2017). The present study provides new information about the chemotaxis of CB in environments other than sediments, revealing key conditions for their attachment to surfaces and growth in both natural and engineered environments

Study site and sediment collection
Sediment incubation
Reactor configuration and operation
Microelectrode measurements
CARD-FISH
Microbial community characterizations
Cable bacteria activity in the sediments of Yaquina Bay
Encouraging the growth of cable bacteria on poised electrodes
Examining the attachment of cable bacteria on the anode
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