In recent years, the externalization of electrons as part of respiratory metabolic processes has been discovered in many different bacteria and some archaea. Microbial extracellular electron transfer (EET) plays an important role in many anoxic natural or engineered ecosystems. In this study, an anaerobic methane-converting microbial community was investigated with regard to its potential to perform EET. At this point, it is not well-known if or how EET confers a competitive advantage to certain species in methane-converting communities. EET was investigated in a two-chamber electrochemical system, sparged with methane and with an applied potential of +400 mV versus standard hydrogen electrode. A biofilm developed on the working electrode and stable low-density current was produced, confirming that EET indeed did occur. The appearance and presence of redox centers at −140 to −160 mV and at −230 mV in the biofilm was confirmed by cyclic voltammetry scans. Metagenomic analysis and fluorescence in situ hybridization of the biofilm showed that the anaerobic methanotroph ‘Candidatus Methanoperedens BLZ2’ was a significant member of the biofilm community, but its relative abundance did not increase compared to the inoculum. On the contrary, the relative abundance of other members of the microbial community significantly increased (up to 720-fold, 7.2% of mapped reads), placing these microorganisms among the dominant species in the bioanode community. This group included Zoogloea sp., Dechloromonas sp., two members of the Bacteroidetes phylum, and the spirochete Leptonema sp. Genes encoding proteins putatively involved in EET were identified in Zoogloea sp., Dechloromonas sp. and one member of the Bacteroidetes phylum. We suggest that instead of methane, alternative carbon sources such as acetate were the substrate for EET. Hence, EET in a methane-driven chemolithoautotrophic microbial community seems a complex process in which interactions within the microbial community are driving extracellular electron transfer to the electrode.
Bibliographical noteKAUST Repository Item: Exported on 2021-06-17
Acknowledged KAUST grant number(s): FCC/1/1971-33-01
Acknowledgements: The authors gratefully acknowledge funding by the Dutch Research Council through the Soehngen Institute for Anaerobic Microbiology (SIAM) Gravitation Grant 024.002.002 (MJ, JF, CUW and HO), ALWOP.293 (SB and CUW) and the Netherlands Earth System Science Center (NESSC) Gravitation Grant 024.002.001 (MJ, MitZ). Furthermore, MJ was supported by the European Research Council (ERC) Advanced Grant Ecology of Anaerobic Methane-oxidizing Microbes (EcoMoM) 339880. TB was supported by the ERC Advanced Grant Volcano 669371. DRS was supported by the Center Competitive Funding Program (FCC/1/1971-33-01) to Pascal E. Saikaly from King Abdullah University of Science and Technology (KAUST). The authors would further like to thank Amelia Rotaru and Mon Oo Yee (University of Southern Denmark) for their help in getting the project started. Gizem Ölcücü contributed by testing different experimental set-ups and Theo van Alen (Radboud University Nijmegen) generated raw sequencing data
This publication acknowledges KAUST support, but has no KAUST affiliated authors.