skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 CO 2 reduction pathway, HdrABC complexed with hydrogenase or formate dehydrogenase generates reduced ferredoxin (Fdx 2-) for the endergonic reduction of CO 2 coupled to the exergonic reduction of CoMS–SCoB dependent on FBEB of electrons from H 2 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 H 2. The HdrABC complexes catalyze FBEB-dependent oxidation of H 2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx 2- supplies electrons for reduction of the methyl group to methane. In H 2- independent pathways, three-fourths of the methyl groups are oxidized producing Fdx 2- and reduced coenzyme F 420 (F 420H 2). The F 420H 2 donates electrons for reduction of the remaining methyl groups to methane requiring transfer of electrons from Fdx 2-more » to F 420. HdrA1B1C1 is proposed to catalyze FBEB-dependent oxidation of Fdx 2- for the endergonic reduction of F 420 driven by the exergonic reduction of CoMS–SCoB. In H 2- 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 Fdx 2- and generates a Na + gradient driving ATP synthesis. It is postulated that F 420 is reduced by Rnf requiring HdrA2B2C2 catalyzing FBEB-dependent oxidation of F 420H 2 for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS–SCoB. The Fdx 2- 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 Fdx 2- is coupled to reduction of F 420. The F 420H 2 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) (SC-22)
OSTI Identifier:
1510457
Grant/Contract Number:  
FG02-95ER20198
Resource Type:
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. doi:10.3389/fmicb.2018.01322.
Yan, Zhen, and Ferry, James G. Wed . "Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis". United States. doi: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},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

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

Save / Share:

Works referenced in this record:

Bioenergetic studies of Methanosphaera stadtmanae , an obligate H 2 –methanol utilising methanogen
journal, August 1993

  • Sparling, Richard; Blaut, Michael; Gottschalk, Gerhard
  • Canadian Journal of Microbiology, Vol. 39, Issue 8
  • DOI: 10.1139/m93-109

Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling
journal, February 2018


Mechanistic insights into energy conservation by flavin-based electron bifurcation
journal, April 2017

  • Lubner, Carolyn E.; Jennings, David P.; Mulder, David W.
  • Nature Chemical Biology, Vol. 13, Issue 6
  • DOI: 10.1038/nchembio.2348

Response of a Rice Paddy Soil Methanogen to Syntrophic Growth as Revealed by Transcriptional Analyses
journal, May 2014

  • Liu, Pengfei; Yang, Yanxiang; Lü, Zhe
  • Applied and Environmental Microbiology, Vol. 80, Issue 15
  • DOI: 10.1128/AEM.01259-14

Products of trace methane oxidation during nonmethyltrophic growth by Methanosarcina
journal, January 2007

  • Moran, James J.; House, Christopher H.; Thomas, B.
  • Journal of Geophysical Research, Vol. 112, Issue G2
  • DOI: 10.1029/2006JG000268

Electron Bifurcation Makes the Puzzle Pieces Fall Energetically into Place in Methanogenic Energy Conservation
journal, November 2017


New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum”
journal, December 2014

  • Lang, Kristina; Schuldes, Jörg; Klingl, Andreas
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03389-14

Functional Role of MrpA in the MrpABCDEFG Na + /H + Antiporter Complex from the Archaeon Methanosarcina acetivorans
journal, October 2016

  • Jasso-Chávez, Ricardo; Diaz-Perez, César; Rodríguez-Zavala, José S.
  • Journal of Bacteriology, Vol. 199, Issue 2
  • DOI: 10.1128/JB.00662-16

Proteome of Methanosarcina a cetivorans Part II:  Comparison of Protein Levels in Acetate- and Methanol-Grown Cells
journal, February 2005

  • Li, Qingbo; Li, Lingyun; Rejtar, Tomas
  • Journal of Proteome Research, Vol. 4, Issue 1
  • DOI: 10.1021/pr049831k

Reverse Methanogenesis and Respiration in Methanotrophic Archaea
journal, January 2017

  • Timmers, Peer H. A.; Welte, Cornelia U.; Koehorst, Jasper J.
  • Archaea, Vol. 2017
  • DOI: 10.1155/2017/1654237

VhuD Facilitates Electron Flow from H2 or Formate to Heterodisulfide Reductase in Methanococcus maripaludis
journal, September 2013

  • Costa, K. C.; Lie, T. J.; Xia, Q.
  • Journal of Bacteriology, Vol. 195, Issue 22
  • DOI: 10.1128/JB.00895-13

Electron transport in acetate-grown Methanosarcina acetivorans
journal, January 2011


Evolution of Na + and H + bioenergetics in methanogenic archaea
journal, February 2013

  • Schlegel, Katharina; Müller, Volker
  • Biochemical Society Transactions, Vol. 41, Issue 1
  • DOI: 10.1042/BST20120294

A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea
journal, December 2015


Promiscuous archaeal ATP synthase concurrently coupled to Na+ and H+ translocation
journal, January 2012

  • Schlegel, K.; Leone, V.; Faraldo-Gomez, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 3
  • DOI: 10.1073/pnas.1115796109

Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004


An unconventional pathway for reduction of CO2 to methane in CO-grown Methanosarcina acetivorans revealed by proteomics
journal, November 2006

  • Lessner, D. J.; Li, L.; Li, Q.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 47
  • DOI: 10.1073/pnas.0608833103

Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase
journal, June 2010

  • Costa, K. C.; Wong, P. M.; Wang, T.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
  • DOI: 10.1073/pnas.1003653107

Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis
journal, August 2012

  • Lie, T. J.; Costa, K. C.; Lupa, B.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 38
  • DOI: 10.1073/pnas.1208779109

How to Make a Living by Exhaling Methane
journal, October 2010


The F420-Reducing [NiFe]-Hydrogenase Complex from Methanothermobacter marburgensis, the First X-ray Structure of a Group 3 Family Member
journal, July 2014

  • Vitt, Stella; Ma, Kesen; Warkentin, Eberhard
  • Journal of Molecular Biology, Vol. 426, Issue 15
  • DOI: 10.1016/j.jmb.2014.05.024

Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen
journal, March 2016

  • Nobu, Masaru Konishi; Narihiro, Takashi; Kuroda, Kyohei
  • The ISME Journal, Vol. 10, Issue 10
  • DOI: 10.1038/ismej.2016.33

MrpA Functions in Energy Conversion during Acetate-Dependent Growth of Methanosarcina acetivorans
journal, July 2013

  • Jasso-Chavez, R.; Apolinario, E. E.; Sowers, K. R.
  • Journal of Bacteriology, Vol. 195, Issue 17
  • DOI: 10.1128/JB.00581-13

Methane and nitrous oxide emissions from the ocean: A reassessment using basin-wide observations in the Atlantic
journal, January 2009

  • Rhee, T. S.; Kettle, A. J.; Andreae, M. O.
  • Journal of Geophysical Research, Vol. 114, Issue D12
  • DOI: 10.1029/2008JD011662

Methanogenesis by Methanosarcina acetivorans involves two structurally and functionally distinct classes of heterodisulfide reductase
journal, February 2010


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

  • Kröninger, Lena; Berger, Stefanie; Welte, Cornelia
  • FEBS Journal, Vol. 283, Issue 3
  • DOI: 10.1111/febs.13594

The methanogenic CO2 reducing-and-fixing enzyme is bifunctional and contains 46 [4Fe-4S] clusters
journal, October 2016


Quantitative Proteomic and Microarray Analysis of the Archaeon M ethanosarcina acetivorans Grown with Acetate versus Methanol
journal, February 2007

  • Li, Lingyun; Li, Qingbo; Rohlin, Lars
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr060383l

Metabolic, Phylogenetic, and Ecological Diversity of the Methanogenic Archaea
journal, March 2008

  • Liu, Yuchen; Whitman, William B.
  • Annals of the New York Academy of Sciences, Vol. 1125, Issue 1
  • DOI: 10.1196/annals.1419.019

Exploring Hydrogenotrophic Methanogenesis: a Genome Scale Metabolic Reconstruction of Methanococcus maripaludis
journal, October 2016

  • Richards, Matthew A.; Lie, Thomas J.; Zhang, Juan
  • Journal of Bacteriology, Vol. 198, Issue 24
  • DOI: 10.1128/JB.00571-16

Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation
journal, February 2013

  • Buckel, Wolfgang; Thauer, Rudolf K.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
  • DOI: 10.1016/j.bbabio.2012.07.002

Methanosaeta, the forgotten methanogen?
journal, April 2007


Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens
journal, July 2014

  • Welte, Cornelia; Deppenmeier, Uwe
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
  • DOI: 10.1016/j.bbabio.2013.12.002

Characterization of Energy-Conserving Hydrogenase B in Methanococcus maripaludis
journal, May 2010

  • Major, T. A.; Liu, Y.; Whitman, W. B.
  • Journal of Bacteriology, Vol. 192, Issue 15
  • DOI: 10.1128/JB.01446-09

Trace methane oxidation studied in several Euryarchaeota under diverse conditions
journal, January 2005

  • Moran, James J.; House, Christopher H.; Freeman, Katherine H.
  • Archaea, Vol. 1, Issue 5
  • DOI: 10.1155/2005/650670

Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008

  • Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
  • Nature Reviews Microbiology, Vol. 6, Issue 8
  • DOI: 10.1038/nrmicro1931

Electron Transport in the Pathway of Acetate Conversion to Methane in the Marine Archaeon Methanosarcina acetivorans
journal, December 2005


Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea
journal, January 2011

  • Kaster, A. -K.; Moll, J.; Parey, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 7
  • DOI: 10.1073/pnas.1016761108

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

  • Schlegel, Katharina; Welte, Cornelia; Deppenmeier, Uwe
  • FEBS Journal, Vol. 279, Issue 24
  • DOI: 10.1111/febs.12031

Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction
journal, August 2017


Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea
journal, January 2017


Reversing methanogenesis to capture methane for liquid biofuel precursors
journal, January 2016

  • Soo, Valerie W. C.; McAnulty, Michael J.; Tripathi, Arti
  • Microbial Cell Factories, Vol. 15, Issue 1
  • DOI: 10.1186/s12934-015-0397-z

Acetate Metabolism in Anaerobes from the Domain Archaea
journal, June 2015


Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H 2 Storage
journal, June 2010


Genomic analysis of methanogenic archaea reveals a shift towards energy conservation
journal, August 2017


Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013


A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration
journal, April 2018