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Title: Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis

Abstract

Reduction of the disulfide of coenzyme M and coenzyme B (CoMS–SCoB) by heterodisulfide reductases (HdrED and HdrABC) is the final step in all methanogenic pathways. Flavin-based electron bifurcation (FBEB) by soluble HdrABC homologs play additional roles in driving essential endergonic reactions at the expense of the exergonic reduction of CoMS–SCoM. In the first step of the CO2 reduction pathway, HdrABC complexed with hydrogenase or formate dehydrogenase generates reduced ferredoxin (Fdx2-) for the endergonic reduction of CO2 coupled to the exergonic reduction of CoMS–SCoB dependent on FBEB of electrons from H2 or formate. Roles for HdrABC:hydrogenase complexes are also proposed for pathways wherein the methyl group of methanol is reduced to methane with electrons from H2. The HdrABC complexes catalyze FBEB-dependent oxidation of H2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx2- supplies electrons for reduction of the methyl group to methane. In H2- independent pathways, three-fourths of the methyl groups are oxidized producing Fdx2- and reduced coenzyme F420 (F420H2). The F420H2 donates electrons for reduction of the remaining methyl groups to methane requiring transfer of electrons from Fdx2- to F420. HdrA1B1C1 is proposed to catalyze FBEB-dependent oxidation of Fdx2- for the endergonic reductionmore » of F420 driven by the exergonic reduction of CoMS–SCoB. In H2- independent acetotrophic pathways, the methyl group of acetate is reduced to methane with electrons derived from oxidation of the carbonyl group mediated by Fdx. Electron transport involves a membrane-bound complex (Rnf) that oxidizes Fdx2- and generates a Na+ gradient driving ATP synthesis. It is postulated that F420 is reduced by Rnf requiring HdrA2B2C2 catalyzing FBEB-dependent oxidation of F420H2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx2- is recycled by Rnf and HdrA2B2C2 thereby conserving energy. The HdrA2B2C2 is also proposed to play a role in Fe(III)-dependent reverse methanogenesis. A flavin-based electron confurcating (FBEC) HdrABC complex is proposed for nitrate-dependent reverse methanogenesis in which the oxidation of CoM-SH/CoB-SH and Fdx2- is coupled to reduction of F420. The F420H2 donates electrons to a membrane complex that generates a proton gradient driving ATP synthesis.« less

Authors:
 [1];  [1]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology
Publication Date:
Research Org.:
Pennsylvania State University, State College, PA 16801 (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1510457
Grant/Contract Number:  
FG02-95ER20198
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; archaea; heterodisulfide reductase; methane; ferredoxin; hydrogen; acetate; formate

Citation Formats

Yan, Zhen, and Ferry, James G. Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.01322.
Yan, Zhen, & Ferry, James G. Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis. United States. https://doi.org/10.3389/fmicb.2018.01322
Yan, Zhen, and Ferry, James G. 2018. "Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis". United States. https://doi.org/10.3389/fmicb.2018.01322. https://www.osti.gov/servlets/purl/1510457.
@article{osti_1510457,
title = {Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis},
author = {Yan, Zhen and Ferry, James G.},
abstractNote = {Reduction of the disulfide of coenzyme M and coenzyme B (CoMS–SCoB) by heterodisulfide reductases (HdrED and HdrABC) is the final step in all methanogenic pathways. Flavin-based electron bifurcation (FBEB) by soluble HdrABC homologs play additional roles in driving essential endergonic reactions at the expense of the exergonic reduction of CoMS–SCoM. In the first step of the CO2 reduction pathway, HdrABC complexed with hydrogenase or formate dehydrogenase generates reduced ferredoxin (Fdx2-) for the endergonic reduction of CO2 coupled to the exergonic reduction of CoMS–SCoB dependent on FBEB of electrons from H2 or formate. Roles for HdrABC:hydrogenase complexes are also proposed for pathways wherein the methyl group of methanol is reduced to methane with electrons from H2. The HdrABC complexes catalyze FBEB-dependent oxidation of H2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx2- supplies electrons for reduction of the methyl group to methane. In H2- independent pathways, three-fourths of the methyl groups are oxidized producing Fdx2- and reduced coenzyme F420 (F420H2). The F420H2 donates electrons for reduction of the remaining methyl groups to methane requiring transfer of electrons from Fdx2- to F420. HdrA1B1C1 is proposed to catalyze FBEB-dependent oxidation of Fdx2- for the endergonic reduction of F420 driven by the exergonic reduction of CoMS–SCoB. In H2- independent acetotrophic pathways, the methyl group of acetate is reduced to methane with electrons derived from oxidation of the carbonyl group mediated by Fdx. Electron transport involves a membrane-bound complex (Rnf) that oxidizes Fdx2- and generates a Na+ gradient driving ATP synthesis. It is postulated that F420 is reduced by Rnf requiring HdrA2B2C2 catalyzing FBEB-dependent oxidation of F420H2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx2- is recycled by Rnf and HdrA2B2C2 thereby conserving energy. The HdrA2B2C2 is also proposed to play a role in Fe(III)-dependent reverse methanogenesis. A flavin-based electron confurcating (FBEC) HdrABC complex is proposed for nitrate-dependent reverse methanogenesis in which the oxidation of CoM-SH/CoB-SH and Fdx2- is coupled to reduction of F420. The F420H2 donates electrons to a membrane complex that generates a proton gradient driving ATP synthesis.},
doi = {10.3389/fmicb.2018.01322},
url = {https://www.osti.gov/biblio/1510457}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 9,
place = {United States},
year = {Wed Jun 20 00:00:00 EDT 2018},
month = {Wed Jun 20 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
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Citation Metrics:
Cited by: 37 works
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Figures / Tables:

FIGURE 1 FIGURE 1: | The global carbon cycle. Solid lines indicate aerobic (red) and anaerobic (blue) steps in the cycle and dotted lines indicate transfer of material between aerobic and anaerobic environments. (1) Photosynthesis, (2) aerobic decomposition, (3) fermentation, (4) syntrophic acetogenesis, (5) CO2 reduction to methane with electrons derived frommore » formate or H2, (6) acetotrophic methanogenesis, (7) anerobic oxidation of methane, and (8) aerobic oxidation of methane.« less

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Works referenced in this record:

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Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction
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A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration
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An unconventional pathway for reduction of CO2 to methane in CO-grown Methanosarcina acetivorans revealed by proteomics
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Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase
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Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea
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Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis
journal, August 2012


Electron transport during aceticlastic methanogenesis by Methanosarcina acetivorans involves a sodium-translocating Rnf complex
journal, November 2012


Evidence for the involvement of two heterodisulfide reductases in the energy-conserving system of Methanomassiliicoccus luminyensis
journal, December 2015


Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction
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Response of a Rice Paddy Soil Methanogen to Syntrophic Growth as Revealed by Transcriptional Analyses
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Functional Role of MrpA in the MrpABCDEFG Na + /H + Antiporter Complex from the Archaeon Methanosarcina acetivorans
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Bioenergetic studies of Methanosphaera stadtmanae , an obligate H 2 –methanol utilising methanogen
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Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H 2 Storage
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How to Make a Living by Exhaling Methane
journal, October 2010


Trace methane oxidation studied in several Euryarchaeota under diverse conditions
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Electron transport in acetate-grown Methanosarcina acetivorans
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Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
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Reversing methanogenesis to capture methane for liquid biofuel precursors
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Metabolic, Phylogenetic, and Ecological Diversity of the Methanogenic Archaea
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A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea
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Works referencing / citing this record:

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
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Electron bifurcation: progress and grand challenges
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Methanogens: pushing the boundaries of biology
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One-megadalton metalloenzyme complex in Geobacter metallireducens involved in benzene ring reduction beyond the biological redox window
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Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei
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Methane-Linked Mechanisms of Electron Uptake from Cathodes by Methanosarcina barkeri
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Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer
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Responses of Methanosarcina barkeri to acetate stress
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Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer
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