Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen
Abstract
Although two-thirds of the nearly 1 billion metric tons of methane produced annually in Earth’s biosphere derives from acetate, the in situ process has escaped rigorous understanding. The unresolved question concerns the mechanism by which the exceptionally marginal amount of available energy supports acetotrophic growth of methanogenic archaea in the environment. Here, we show that Methanosarcina acetivorans conserves energy by Fe(III)-dependent respiratory metabolism of acetate, augmenting production of the greenhouse gas methane. An extensively revised, ecologically relevant, biochemical pathway for acetotrophic growth is presented, in which the conservation of respiratory energy is maximized by electron bifurcation, a previously unknown mechanism of biological energy coupling. The results transform the ecological and biochemical understanding of methanogenesis and the role of iron in the mineralization of organic matter in anaerobic environments.
- Authors:
-
- Pennsylvania State Univ., University Park, PA (United States)
- Publication Date:
- Research Org.:
- Pennsylvania State Univ., University Park, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1610282
- Grant/Contract Number:
- FG02-95ER20198
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Science Advances
- Additional Journal Information:
- Journal Volume: 5; Journal Issue: 8; Journal ID: ISSN 2375-2548
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Science & Technology - Other Topics; Ecology
Citation Formats
Prakash, Divya, Chauhan, Shikha S., and Ferry, James G. Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen. United States: N. p., 2019.
Web. doi:10.1126/sciadv.aaw9059.
Prakash, Divya, Chauhan, Shikha S., & Ferry, James G. Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen. United States. https://doi.org/10.1126/sciadv.aaw9059
Prakash, Divya, Chauhan, Shikha S., and Ferry, James G. Wed .
"Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen". United States. https://doi.org/10.1126/sciadv.aaw9059. https://www.osti.gov/servlets/purl/1610282.
@article{osti_1610282,
title = {Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen},
author = {Prakash, Divya and Chauhan, Shikha S. and Ferry, James G.},
abstractNote = {Although two-thirds of the nearly 1 billion metric tons of methane produced annually in Earth’s biosphere derives from acetate, the in situ process has escaped rigorous understanding. The unresolved question concerns the mechanism by which the exceptionally marginal amount of available energy supports acetotrophic growth of methanogenic archaea in the environment. Here, we show that Methanosarcina acetivorans conserves energy by Fe(III)-dependent respiratory metabolism of acetate, augmenting production of the greenhouse gas methane. An extensively revised, ecologically relevant, biochemical pathway for acetotrophic growth is presented, in which the conservation of respiratory energy is maximized by electron bifurcation, a previously unknown mechanism of biological energy coupling. The results transform the ecological and biochemical understanding of methanogenesis and the role of iron in the mineralization of organic matter in anaerobic environments.},
doi = {10.1126/sciadv.aaw9059},
journal = {Science Advances},
number = 8,
volume = 5,
place = {United States},
year = {Wed Aug 21 00:00:00 EDT 2019},
month = {Wed Aug 21 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling
journal, February 2018
- Buckel, Wolfgang; Thauer, Rudolf K.
- Chemical Reviews, Vol. 118, Issue 7
Methanogenic burst in the end-Permian carbon cycle
journal, March 2014
- Rothman, D. H.; Fournier, G. P.; French, K. L.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
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
Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism
journal, November 1987
- Lovley, Derek R.; Stolz, John F.; Nord, Gordon L.
- Nature, Vol. 330, Issue 6145
Coupling of ATP synthesis and methane formation from methanol and molecular hydrogen in Methanosarcina barkeri
journal, May 1984
- Blaut, Michael; Gottschalk, Gerhard
- European Journal of Biochemistry, Vol. 141, Issue 1
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity
journal, January 1993
- Sowers, Kevin R.; Boone, Jane E.; Gunsalus, Robert P.
- Applied and Environmental Microbiology, Vol. 59, Issue 11
MrpA Functions in Energy Conversion during Acetate-Dependent Growth of Methanosarcina acetivorans
journal, February 2014
- Jasso-Chávez, Ricardo; Apolinario, Ethel E.; Sowers, Kevin R.
- Journal of Bacteriology, Vol. 196, Issue 3
Methanogens rapidly transition from methane production to iron reduction
journal, January 2016
- Sivan, O.; Shusta, S. S.; Valentine, D. L.
- Geobiology, Vol. 14, Issue 2
Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones
journal, February 2002
- Bond, Daniel R.; Lovley, Derek R.
- Environmental Microbiology, Vol. 4, Issue 2
Improved identification of methanogenic bacteria by fluorescence microscopy
journal, November 1978
- Doddema, H. J.; Vogels, G. D.
- Applied and Environmental Microbiology, Vol. 36, Issue 5
Sulfate-Dependent Interspecies H2 Transfer between Methanosarcina barkeri and Desulfovibrio vulgaris during Coculture Metabolism of Acetate or Methanol
journal, January 1985
- Phelps, T. J.; Conrad, R.; Zeikus, J. G.
- Applied and Environmental Microbiology, Vol. 50, Issue 3
Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens
journal, June 2014
- Yamada, Chihaya; Kato, Souichiro; Kimura, Satoshi
- FEMS Microbiology Ecology, Vol. 89, Issue 3
A Ferredoxin- and F 420 H 2 -Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea
journal, February 2017
- Yan, Zhen; Wang, Mingyu; Ferry, James G.
- mBio, Vol. 8, Issue 1
Electron transport in acetate-grown Methanosarcina acetivorans
journal, January 2011
- Wang, Mingyu; Tomb, Jean-Francois; Ferry, James G.
- BMC Microbiology, Vol. 11, Issue 1
Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens
journal, June 2014
- Yamada, Chihaya; Kato, Souichiro; Kimura, Satoshi
- FEMS Microbiology Ecology, Vol. 89, Issue 3
Methanogens: reevaluation of a unique biological group.
journal, January 1979
- Balch, W. E.; Fox, G. E.; Magrum, L. J.
- Microbiological Reviews, Vol. 43, Issue 2
Archaeal Community Structure and Pathway of Methane Formation on Rice Roots
journal, January 2004
- Chin, K. -J.; Lueders, T.; Friedrich, M. W.
- Microbial Ecology, Vol. 47, Issue 1
Coupling of ATP synthesis and methane formation from methanol and molecular hydrogen in Methanosarcina barkeri
journal, May 1984
- Blaut, Michael; Gottschalk, Gerhard
- European Journal of Biochemistry, Vol. 141, Issue 1
Dissimilatory Fe(III) Reduction by the Marine Microorganism Desulfuromonas acetoxidans
journal, January 1993
- Roden, Eric E.; Lovley, Derek R.
- Applied and Environmental Microbiology, Vol. 59, Issue 3
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
Assessment of the oxidant tolerance of Methanosarcina acetivorans
journal, March 2013
- Horne, Alexandra J.; Lessner, Daniel J.
- FEMS Microbiology Letters, Vol. 343, Issue 1
Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron and sulfate and to methanogenesis in anoxic rice field soil
journal, January 2000
- Chidthaisong, Amnat; Conrad, Ralf
- FEMS Microbiology Ecology, Vol. 31, Issue 1
Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling
journal, February 2018
- Buckel, Wolfgang; Thauer, Rudolf K.
- Chemical Reviews, Vol. 118, Issue 7
The global methane cycle: recent advances in understanding the microbial processes involved: Global methane cycle
journal, June 2009
- Conrad, Ralf
- Environmental Microbiology Reports, Vol. 1, Issue 5
Methanosarcina acetivorans sp. nov., an Acetotrophic Methane-Producing Bacterium Isolated from Marine Sediments
journal, January 1984
- Sowers, Kevin R.; Baron, Stephen F.; Ferry, James G.
- Applied and Environmental Microbiology, Vol. 47, Issue 5
Organic Matter Mineralization with Reduction of Ferric Iron in Anaerobic Sediments
journal, January 1986
- Lovley, Derek R.; Phillips, Elizabeth J. P.
- Applied and Environmental Microbiology, Vol. 51, Issue 4
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
Geochemical drivers of organic matter decomposition in arctic tundra soils
journal, December 2015
- Herndon, Elizabeth M.; Yang, Ziming; Bargar, John
- Biogeochemistry, Vol. 126, Issue 3
A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration
journal, April 2018
- Yan, Zhen; Joshi, Prachi; Gorski, Christopher A.
- Nature Communications, Vol. 9, Issue 1
Hydrogen ?leakage? during methanogenesis from methanol and methylamine: implications for anaerobic carbon degradation pathways in aquatic sediments
journal, April 2007
- Finke, Niko; Hoehler, Tori Michael; Jørgensen, Bo Barker
- Environmental Microbiology, Vol. 9, Issue 4
Assessment of the oxidant tolerance of Methanosarcina acetivorans
journal, March 2013
- Horne, Alexandra J.; Lessner, Daniel J.
- FEMS Microbiology Letters, Vol. 343, Issue 1
Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese
journal, January 1988
- Lovley, Derek R.; Phillips, Elizabeth J. P.
- Applied and Environmental Microbiology, Vol. 54, Issue 6
Effects of Amendment with Ferrihydrite and Gypsum on the Structure and Activity of Methanogenic Populations in Rice Field Soil
journal, May 2002
- Lueders, T.; Friedrich, M. W.
- Applied and Environmental Microbiology, Vol. 68, Issue 5
Methane Biogeochemistry and Methanogen Communities in Two Northern Peatland Ecosystems, New York State
journal, November 2003
- Basiliko, N.; Yavitt, J. B.; Dees, P. M.
- Geomicrobiology Journal, Vol. 20, Issue 6
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
ZOLA-3D allows flexible 3D localization microscopy over an adjustable axial range
journal, June 2018
- Aristov, Andrey; Lelandais, Benoit; Rensen, Elena
- Nature Communications, Vol. 9, Issue 1
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
Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron and sulfate and to methanogenesis in anoxic rice field soil
journal, January 2000
- Chidthaisong, Amnat; Conrad, Ralf
- FEMS Microbiology Ecology, Vol. 31, Issue 1
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
Methanogens rapidly transition from methane production to iron reduction
journal, January 2016
- Sivan, O.; Shusta, S. S.; Valentine, D. L.
- Geobiology, Vol. 14, Issue 2
Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments
journal, December 1996
- Roden, Eric E.; Wetzel, Robert G.
- Limnology and Oceanography, Vol. 41, Issue 8
Hydrogen ?leakage? during methanogenesis from methanol and methylamine: implications for anaerobic carbon degradation pathways in aquatic sediments
journal, April 2007
- Finke, Niko; Hoehler, Tori Michael; Jørgensen, Bo Barker
- Environmental Microbiology, Vol. 9, Issue 4
Effect of ferrihydrite biomineralization on methanogenesis in an anaerobic incubation from paddy soil: IRON MINERALIZATION AND METHANOGENESIS
journal, May 2015
- Zhuang, Li; Xu, Jielong; Tang, Jia
- Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 5
Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones
journal, February 2002
- Bond, Daniel R.; Lovley, Derek R.
- Environmental Microbiology, Vol. 4, Issue 2
Dissimilatory Fe(III) Reduction by the Marine Microorganism Desulfuromonas acetoxidans
journal, January 1993
- Roden, Eric E.; Lovley, Derek R.
- Applied and Environmental Microbiology, Vol. 59, Issue 3
A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration
journal, April 2018
- Yan, Zhen; Joshi, Prachi; Gorski, Christopher A.
- Nature Communications, Vol. 9, Issue 1
Sulfate-Dependent Interspecies H2 Transfer between Methanosarcina barkeri and Desulfovibrio vulgaris during Coculture Metabolism of Acetate or Methanol
journal, January 1985
- Phelps, T. J.; Conrad, R.; Zeikus, J. G.
- Applied and Environmental Microbiology, Vol. 50, Issue 3
Methanogens: reevaluation of a unique biological group.
journal, January 1979
- Balch, W. E.; Fox, G. E.; Magrum, L. J.
- Microbiological Reviews, Vol. 43, Issue 2
A Serum Bottle Modification of the Hungate Technique for Cultivating Obligate Anaerobes
journal, January 1974
- Miller, Terry L.; Wolin, M. J.
- Applied Microbiology, Vol. 27, Issue 5
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity
journal, January 1993
- Sowers, Kevin R.; Boone, Jane E.; Gunsalus, Robert P.
- Applied and Environmental Microbiology, Vol. 59, Issue 11
Improved identification of methanogenic bacteria by fluorescence microscopy
journal, November 1978
- Doddema, H. J.; Vogels, G. D.
- Applied and Environmental Microbiology, Vol. 36, Issue 5
Organic Matter Mineralization with Reduction of Ferric Iron in Anaerobic Sediments
journal, January 1986
- Lovley, Derek R.; Phillips, Elizabeth J. P.
- Applied and Environmental Microbiology, Vol. 51, Issue 4
Works referencing / citing this record:
High-Level Abundances of Methanobacteriales and Syntrophobacterales May Help To Prevent Corrosion of Metal Sheet Piles
journal, August 2019
- in ‘t Zandt, Michiel H.; Kip, Nardy; Frank, Jeroen
- Applied and Environmental Microbiology, Vol. 85, Issue 20
Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei
journal, October 2019
- Wang, Hui; Byrne, James M.; Liu, Pengfei
- Environmental Microbiology Reports, Vol. 12, Issue 1
Structure and function of an unusual flavodoxin from the domain Archaea
journal, December 2019
- Prakash, Divya; Iyer, Prashanti R.; Suharti, Suharti
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 51