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Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri

Kulkarni, Gargi and Mand, Thomas D. and Metcalf, William W. (2018) Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri. mBio, 9 (4). Art. No. e01256-18. ISSN 2150-7511. PMCID PMC6030560. https://resolver.caltech.edu/CaltechAUTHORS:20180919-164643210

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Abstract

Energy conservation via hydrogen cycling, which generates proton motive force by intracellular H_2 production coupled to extracellular consumption, has been controversial since it was first proposed in 1981. It was hypothesized that the methanogenic archaeon Methanosarcina barkeri is capable of energy conservation via H_2 cycling, based on genetic data that suggest that H_2 is a preferred, but nonessential, intermediate in the electron transport chain of this organism. Here, we characterize a series of hydrogenase mutants to provide direct evidence of H_2 cycling. M. barkeri produces H_2 during growth on methanol, a phenotype that is lost upon mutation of the cytoplasmic hydrogenase encoded by frhADGB, although low levels of H_2, attributable to the Ech hydrogenase, accumulate during stationary phase. In contrast, mutations that conditionally inactivate the extracellular Vht hydrogenase are lethal when expression of the vhtGACD operon is repressed. Under these conditions, H_2 accumulates, with concomitant cessation of methane production and subsequent cell lysis, suggesting that the inability to recapture extracellular H_2 is responsible for the lethal phenotype. Consistent with this interpretation, double mutants that lack both Vht and Frh are viable. Thus, when intracellular hydrogen production is abrogated, loss of extracellular H_2 consumption is no longer lethal. The common occurrence of both intracellular and extracellular hydrogenases in anaerobic microorganisms suggests that this unusual mechanism of energy conservation may be widespread in nature.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mbio.01256-18DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6030560/PubMed CentralArticle
https://doi.org/10.1101/335794DOIDiscussion Paper
ORCID:
AuthorORCID
Metcalf, William W.0000-0002-0182-0671
Additional Information:© 2018 Kulkarni et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 8 June 2018. Accepted 11 June 2018. Published 3 July 2018. We thank Rob Sanford for providing assistance and facilities for measurement of low hydrogen partial pressures. We acknowledge the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through grant DE-FG02-02ER15296 for funding this work. This article is a direct contribution from a Fellow of the American Academy of Microbiology. Solicited external reviewers: Rudolf Thauer, Max Planck Institute for Terrestrial Microbiology; Derek Lovley, University of Massachusetts Amherst.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-FG02-02ER15296
Subject Keywords:Methanosarcina, energy conservation, hydrogenase, methanogenesis
Issue or Number:4
PubMed Central ID:PMC6030560
Record Number:CaltechAUTHORS:20180919-164643210
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180919-164643210
Official Citation:Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri Gargi Kulkarni, Thomas D. Mand, William W. Metcalf mBio Jul 2018, 9 (4) e01256-18; DOI: 10.1128/mBio.01256-18
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:89770
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:20 Sep 2018 14:30
Last Modified:03 Oct 2019 20:19

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