Mechanisms for Electron Uptake by Methanosarcina acetivorans during Direct Interspecies Electron Transfer.

Content Provider	Europe PMC
Author	Holmes, Dawn E. Zhou, Jinjie Ueki, Toshiyuki Woodard, Trevor Lovley, Derek R.
Editor	Papoutsakis, Eleftherios T.
Copyright Year	2021
Abstract	ABSTRACTDirect interspecies electron transfer (DIET) between bacteria and methanogenic archaea appears to be an important syntrophy in both natural and engineered methanogenic environments. However, the electrical connections on the outer surface of methanogens and the subsequent processing of electrons for carbon dioxide reduction to methane are poorly understood. Here, we report that the genetically tractable methanogen Methanosarcina acetivorans can grow via DIET in coculture with Geobacter metallireducens serving as the electron-donating partner. Comparison of gene expression patterns in M. acetivorans grown in coculture versus pure-culture growth on acetate revealed that transcripts for the outer-surface multiheme c-type cytochrome MmcA were higher during DIET-based growth. Deletion of mmcA inhibited DIET. The high aromatic amino acid content of M. acetivorans archaellins suggests that they might assemble into electrically conductive archaella. A mutant that could not express archaella was deficient in DIET. However, this mutant grew in DIET-based coculture as well as the archaellum-expressing parental strain in the presence of granular activated carbon, which was previously shown to serve as a substitute for electrically conductive pili as a conduit for long-range interspecies electron transfer in other DIET-based cocultures. Transcriptomic data suggesting that the membrane-bound Rnf, Fpo, and HdrED complexes also play a role in DIET were incorporated into a charge-balanced model illustrating how electrons entering the cell through MmcA can yield energy to support growth from carbon dioxide reduction. The results are the first genetics-based functional demonstration of likely outer-surface electrical contacts for DIET in a methanogen.
Page Count	12
Journal	Mbio
Volume Number	12
PubMed Central reference number	PMC8546582
Issue Number	5
PubMed reference number	34607451
e-ISSN	21507511
DOI	10.1128/mbio.02344-21
Language	English
Publisher	American Society for Microbiology
Publisher Date	2021-10-05
Publisher Place	1752 N St., N.W., Washington, DC
Access Restriction	Open
Rights License	This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Copyright © 2021 Holmes et al.
Subject Keyword	anaerobic respiration extracellular electron transfer Methanosarcina Geobacter direct interspecies electron transfer DIET Rnf complex c-type cytochrome methanogen archaea
Content Type	Text
Resource Type	Article
Subject	Microbiology Virology