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Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri

Journal Article · · mBio (Online)
 [1];  [2];  [2];  [3]
  1. Univ. of California, Irvine, CA (United States); California Inst. of Technology (CalTech), Pasadena, CA (United States); Univ. of Illinois, Urbana, IL (United States)
  2. Univ. of Illinois, Champaign, IL (United States)
  3. Univ. of California, Irvine, CA (United States)
+ Show Author Affiliations

Energy conservation via hydrogen cycling, which generates proton motive force by intracellular H2production coupled to extracellular consumption, has been controversial since it was first proposed in 1981. It was hypothesized that the methanogenic archaeonMethanosarcina barkeriis capable of energy conservation via H2cycling, based on genetic data that suggest that H2is 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 H2cycling.M. barkeriproduces H2during growth on methanol, a phenotype that is lost upon mutation of the cytoplasmic hydrogenase encoded byfrhADGB, although low levels of H2, attributable to the Ech hydrogenase, accumulate during stationary phase. In contrast, mutations that conditionally inactivate the extracellular Vht hydrogenase are lethal when expression of thevhtGACDoperon is repressed. Under these conditions, H2accumulates, with concomitant cessation of methane production and subsequent cell lysis, suggesting that the inability to recapture extracellular H2is 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 H2 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.

IMPORTANCE

ATP is required by all living organisms to facilitate essential endergonic reactions required for growth and maintenance. Although synthesis of ATP by substrate-level phosphorylation is widespread and significant, most ATP is made via the enzyme ATP synthase, which is energized by transmembrane chemiosmotic gradients. Therefore, establishing this gradient across the membrane is of central importance to sustaining life. Experimental validation of H2cycling adds to a short list of mechanisms for generating a transmembrane electrochemical gradient that is likely to be widespread, especially among anaerobic microorganisms.

Research Organization:
Univ. of Illinois, Champaign, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
FG02-02ER15296
OSTI ID:
1510523
Alternate ID(s):
OSTI ID: 1595341
Journal Information:
mBio (Online), Journal Name: mBio (Online) Journal Issue: 4 Vol. 9; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (16)

The hydrogen threshold of obligately methyl-reducing methanogens journal August 2020
Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer journal December 2018
NanoFe3O4 as Solid Electron Shuttles to Accelerate Acetotrophic Methanogenesis by Methanosarcina barkeri journal March 2019
Transcriptomic response during wasp parasitism in the Drosophila-Spiroplasma interaction collection January 2020
Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes journal January 2020
Compositional and functional differences of the mucosal microbiota along the intestine of healthy individuals journal September 2020
Methanogens: pushing the boundaries of biology journal December 2018
Unique subsite specificity and potential natural function of a chitosan deacetylase from the human pathogen Cryptococcus neoformans journal February 2020
Increasing sulfate levels show a differential impact on synthetic communities comprising different methanogens and a sulfate reducer journal May 2019
Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei journal October 2019
Genetic, Biochemical, and Molecular Characterization of Methanosarcina barkeri Mutants Lacking Three Distinct Classes of Hydrogenase journal July 2018
The Hydrogen Economy of Methanosarcina barkeri : Life in the Fast Lane journal August 2018
Energy Conservation and Hydrogenase Function in Methanogenic Archaea, in Particular the Genus Methanosarcina journal September 2019
Responses of Methanosarcina barkeri to acetate stress journal December 2019
Streptococcal Lancefield polysaccharides are critical cell wall determinants for human Group IIA secreted phospholipase A2 to exert its bactericidal effects journal October 2018
Extracellular Electron Uptake by Two Methanosarcina Species journal April 2019

Figures / Tables (4)

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Methanosarcina
energy conservation
hydrogenase
methanogenesis