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Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

He, Xiaojia and Chadwick, Grayson L. and Kempes, Christopher P. and Orphan, Victoria J. and Meile, Christof (2021) Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia. mBio, 12 (3). Art. No. e03620-20. ISSN 2150-7511. doi:10.1128/mBio.03620-20.

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About 382 Tg yr⁻¹ of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007,, preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia.

Item Type:Article
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URLURL TypeDescription
He, Xiaojia0000-0001-8274-5564
Chadwick, Grayson L.0000-0003-0700-9350
Orphan, Victoria J.0000-0002-5374-6178
Meile, Christof0000-0002-0825-4596
Additional Information:© 2021 He et al. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 7 January 2021; Accepted 15 March 2021; Published 11 May 2021. This work was supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program, under award numbers DE‐SC0016469 and DE-SC0020373 (to C.M. and V.J.O.) and DE-SC0016469 (subaward S390693 to C.P.K.) and by a grant from the Simons Foundation collaboration on Principles of Microbial Ecosystems (PriME; to V.J.O.). Samples for this study were collected during a research expedition funded by the National Science Foundation grant number OCE 1634002 (to V.J.O.). We thank Roland Hatzenpichler for his contributions to the ANME-2b FISH probe design and Yunbin Guan for his assistance with the nanoSIMS analysis. We have no conflict of interest to declare.
Funding AgencyGrant Number
Department of Energy (DOE)DE‐SC0016469
Department of Energy (DOE)DE-SC0020373
Department of Energy (DOE)DE-SC0016469
Department of Energy (DOE)S390693
Simons FoundationUNSPECIFIED
Subject Keywords:syntrophy; FISH-nanoSIMS; activation loss; anaerobic oxidation of methane; conductive network density; conductivity; direct interspecies electron transfer; electron conduction; ohmic resistance; spatial statistics; stable isotope probing; syntrophy
Issue or Number:3
Record Number:CaltechAUTHORS:20210517-093742807
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Official Citation:Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia. Xiaojia He, Grayson L. Chadwick, Christopher P. Kempes, Victoria J. Orphan, Christof Meile. mBio May 2021, 12 (3) e03620-20; DOI: 10.1128/mBio.03620-20
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109144
Deposited By: Tony Diaz
Deposited On:17 May 2021 16:50
Last Modified:17 May 2021 16:50

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