Electrochemical and phylogenetic comparisons of oxygen-reducing electroautotrophic communities

Fundamental knowledge on oxygen-reducing microbial cathodes is scarce, for instance on the mechanisms of extracellular electron transfer or on the microbial taxa proposed to induce the electroactivity that are commonly unclassified representatives of the Gammaproteobacteria abundantly found in these communities. Here we first investigate electroactive biofilms (EABs) grown on carbon electrodes at +0.20V vs. Ag/AgCl under air and attest their apparent 'electroautotrophic' behavior. The EABs catalyzed O2 electroreduction into water - as confirmed by a rotating ring disc experiment - and performed quasi-reversible heterogeneous electron transfer (HET). By using electrodes of low surface capacitance, we report for the first time nonturnover redox peaks that are very likely intrinsic to the redox protein(s) performing the HET. Because the formal potential of redox proteins is pH-dependent, we investigated the evolution with the solution pH of characteristic potentials for the EABs: (i) open circuit potential, (ii) half-wave potential, and (iii) averaged peak potential of nonturnover cyclic voltammograms, which is presumably the formal potential of the primary electron acceptor(s) for the community. In addition to help understanding the redox thermodynamics behind the HET, we suggest that the corresponding data provide an electrochemical fingerprinting that could help comparing the electroactivity of diverse microbial communities. The taxon with the highest relative abundance in our EABs was an unclassified member of the Gammaproteobacterial. It was phylogenetically closely related with most other abundant unclassified Gammaproteobacteria reported in O2 reducing EABs, further suggesting that those taxa are responsible for the bioelectroactivity. Jointly, phylogenetic and electrochemical similarities between reported EABs support the hypothesis that similar biomolecular mechanisms may be at stake for this - highly probable - electroautotrophic metabolism.