Co-occurrence of Direct and Indirect Extracellular Electron Transfer Mechanisms during Electroactive Respiration in a Dissimilatory Sulfate Reducing Bacterium

Abstract

Extracellular electron transfer (EET) propels microbial fuel cell (MFC) technology and contributes to the mobility of redox active minerals and microbial syntrophy in nature. Although extensive studies on Sulfate-reducing bacteria (SRB)-mediated metal electrode corrosion have been done, there remain knowledge gaps on SRB EET to electrodes. Our MFCs with Desulfovibrio vulgaris Hildenborough (DvH), a model SRB, indicated that DvH can harvest and send electrons to the carbon cloth electrode. Patterns in current production compared to variations of electron donor/acceptor ratios in the anode and cathode suggested that attachment of DvH to the electrode and biofilm density were critical for effective electricity generation. Analysis of DvH biofilms at different conditions by electron microscopy indicated DvH utilized filaments that resemble nano-pili to attach on electrodes and facilitate EET from cell-to-cell and to the electrode. Proteomics profiling of electroactive respiration proteins indicated DvH adapted to electroactive respiration by presenting more pili-, flagellar- related proteins and histidine kinases on electrodes. The mutant with a deletion of the major pilus-producing gene yielded less voltage and far less attachment to the electrode, suggesting the importance of pili in EET. The mutant with a deficiency in biofilm formation, however, did not eliminate current production indicating the existence of indirect EET. Untargeted metabolomics profiling showed flavin-based metabolites, potential electron shuttles, were dysregulated between respiration modes. This work revealed the metabolic flexibility of DvH to thrive in non-ideal conditions with solid surfaces as both an electron acceptor and donor by using a combination of direct and indirect EET mechanisms.