DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes

Abstract

Twelve evolutionarily unrelated oxidoreductases form enzyme complexes that catalyze the simultaneous coupling of exergonic and endergonic oxidation–reduction reactions to circumvent thermodynamic barriers and minimize free energy loss in a process known as flavin-based electron bifurcation. Common to these 12 bifurcating (Bf) enzymes are protein-bound flavin, the proposed site of bifurcation, and the electron carrier ferredoxin. Despite the documented role of Bf enzymes in balancing the redox state of intracellular electron carriers and in improving the efficiency of cellular metabolism, a comprehensive description of the diversity and evolutionary history of Bf enzymes is lacking. Here, we report the taxonomic distribution, functional diversity, and evolutionary history of Bf enzyme homologs in 4,588 archaeal, bacterial, and eukaryal genomes and 3,136 community metagenomes. Bf homologs were primarily detected in the genomes of anaerobes, including those of sulfate-reducers, acetogens, fermenters, and methanogens. Phylogenetic analyses of Bf enzyme catalytic subunits (oxidoreductases) suggest they were not a property of the Last Universal Common Ancestor of Archaea and Bacteria, which is consistent with the limited and unique taxonomic distributions of enzyme homologs among genomes. Further, phylogenetic analyses of oxidoreductase subunits reveal that non-Bf homologs predate Bf homologs. These observations indicate that multiple independent recruitments of flavoproteins to existingmore » oxidoreductases enabled coupling of numerous new electron Bf reactions. Consistent with the role of these enzymes in the energy metabolism of anaerobes, homologs of Bf enzymes were enriched in metagenomes from subsurface environments relative to those from surface environments. Phylogenetic analyses of homologs from metagenomes reveal that the earliest evolving homologs of most Bf enzymes are from subsurface environments, including fluids from subsurface rock fractures and hydrothermal systems. Collectively, these data suggest strong selective pressures drove the emergence of Bf enzyme complexes via recruitment of flavoproteins that allowed for an increase in the efficiency of cellular metabolism and improvement in energy capture in anaerobes inhabiting a variety of subsurface anoxic habitats where the energy yield of oxidation-reduction reactions is generally low.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Montana State Univ., Bozeman, MT (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1462762
Alternate Identifier(s):
OSTI ID: 1510454
Grant/Contract Number:  
SC0012518
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; electron bifurcation; flavin; ferredoxin; anoxic; subsurface; oxidoreductase; LUCA; metagenomes

Citation Formats

Poudel, Saroj, Dunham, Eric C., Lindsay, Melody R., Amenabar, Maximiliano J., Fones, Elizabeth M., Colman, Daniel R., and Boyd, Eric S. Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes. Switzerland: N. p., 2018. Web. doi:10.3389/fmicb.2018.01762.
Poudel, Saroj, Dunham, Eric C., Lindsay, Melody R., Amenabar, Maximiliano J., Fones, Elizabeth M., Colman, Daniel R., & Boyd, Eric S. Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes. Switzerland. https://doi.org/10.3389/fmicb.2018.01762
Poudel, Saroj, Dunham, Eric C., Lindsay, Melody R., Amenabar, Maximiliano J., Fones, Elizabeth M., Colman, Daniel R., and Boyd, Eric S. Fri . "Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes". Switzerland. https://doi.org/10.3389/fmicb.2018.01762.
@article{osti_1462762,
title = {Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes},
author = {Poudel, Saroj and Dunham, Eric C. and Lindsay, Melody R. and Amenabar, Maximiliano J. and Fones, Elizabeth M. and Colman, Daniel R. and Boyd, Eric S.},
abstractNote = {Twelve evolutionarily unrelated oxidoreductases form enzyme complexes that catalyze the simultaneous coupling of exergonic and endergonic oxidation–reduction reactions to circumvent thermodynamic barriers and minimize free energy loss in a process known as flavin-based electron bifurcation. Common to these 12 bifurcating (Bf) enzymes are protein-bound flavin, the proposed site of bifurcation, and the electron carrier ferredoxin. Despite the documented role of Bf enzymes in balancing the redox state of intracellular electron carriers and in improving the efficiency of cellular metabolism, a comprehensive description of the diversity and evolutionary history of Bf enzymes is lacking. Here, we report the taxonomic distribution, functional diversity, and evolutionary history of Bf enzyme homologs in 4,588 archaeal, bacterial, and eukaryal genomes and 3,136 community metagenomes. Bf homologs were primarily detected in the genomes of anaerobes, including those of sulfate-reducers, acetogens, fermenters, and methanogens. Phylogenetic analyses of Bf enzyme catalytic subunits (oxidoreductases) suggest they were not a property of the Last Universal Common Ancestor of Archaea and Bacteria, which is consistent with the limited and unique taxonomic distributions of enzyme homologs among genomes. Further, phylogenetic analyses of oxidoreductase subunits reveal that non-Bf homologs predate Bf homologs. These observations indicate that multiple independent recruitments of flavoproteins to existing oxidoreductases enabled coupling of numerous new electron Bf reactions. Consistent with the role of these enzymes in the energy metabolism of anaerobes, homologs of Bf enzymes were enriched in metagenomes from subsurface environments relative to those from surface environments. Phylogenetic analyses of homologs from metagenomes reveal that the earliest evolving homologs of most Bf enzymes are from subsurface environments, including fluids from subsurface rock fractures and hydrothermal systems. Collectively, these data suggest strong selective pressures drove the emergence of Bf enzyme complexes via recruitment of flavoproteins that allowed for an increase in the efficiency of cellular metabolism and improvement in energy capture in anaerobes inhabiting a variety of subsurface anoxic habitats where the energy yield of oxidation-reduction reactions is generally low.},
doi = {10.3389/fmicb.2018.01762},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fmicb.2018.01762

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes
journal, November 2010

  • Biegel, Eva; Schmidt, Silke; González, José M.
  • Cellular and Molecular Life Sciences, Vol. 68, Issue 4
  • DOI: 10.1007/s00018-010-0555-8

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

Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis
journal, May 2017


The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth
journal, May 2012


The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor
journal, July 2016

  • Schut, Gerrit J.; Zadvornyy, Oleg; Wu, Chang-Hao
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 7
  • DOI: 10.1016/j.bbabio.2016.01.010

Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments
journal, March 2015

  • D’Hondt, Steven; Inagaki, Fumio; Zarikian, Carlos Alvarez
  • Nature Geoscience, Vol. 8, Issue 4
  • DOI: 10.1038/ngeo2387

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation
journal, June 2015

  • Peters, John W.; Schut, Gerrit J.; Boyd, Eric S.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6
  • DOI: 10.1016/j.bbamcr.2014.11.021

Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds
journal, February 2018

  • Poudel, Saroj; Colman, Daniel R.; Fixen, Kathryn R.
  • Journal of Bacteriology, Vol. 200, Issue 10
  • DOI: 10.1128/JB.00757-17

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

CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


Hydrothermal vents and the origin of life
journal, September 2008

  • Martin, William; Baross, John; Kelley, Deborah
  • Nature Reviews Microbiology, Vol. 6, Issue 11
  • DOI: 10.1038/nrmicro1991

Unification of [FeFe]-hydrogenases into three structural and functional groups
journal, September 2016

  • Poudel, Saroj; Tokmina-Lukaszewska, Monika; Colman, Daniel R.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1860, Issue 9
  • DOI: 10.1016/j.bbagen.2016.05.034

On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation–reduction reactions
journal, January 2018

  • Peters, John W.; Beratan, David N.; Schut, Gerrit J.
  • Chemical Communications, Vol. 54, Issue 33
  • DOI: 10.1039/c8cc01530a

Classification and phylogeny of hydrogenases
journal, August 2001


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

Defining Electron Bifurcation in the Electron-Transferring Flavoprotein Family
journal, August 2017

  • Garcia Costas, Amaya M.; Poudel, Saroj; Miller, Anne-Frances
  • Journal of Bacteriology, Vol. 199, Issue 21
  • DOI: 10.1128/JB.00440-17

The physiology and habitat of the last universal common ancestor
journal, July 2016


Electron Bifurcation: A Long-Hidden Energy-Coupling Mechanism
journal, September 2018


On the Natural History of Flavin-Based Electron Bifurcation
journal, July 2018

  • Baymann, Frauke; Schoepp-Cothenet, Barbara; Duval, Simon
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01357

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Insights into Flavin-based Electron Bifurcation via the NADH-dependent Reduced Ferredoxin:NADP Oxidoreductase Structure
journal, July 2015

  • Demmer, Julius K.; Huang, Haiyan; Wang, Shuning
  • Journal of Biological Chemistry, Vol. 290, Issue 36
  • DOI: 10.1074/jbc.M115.656520

An Electron-bifurcating Caffeyl-CoA Reductase
journal, March 2013

  • Bertsch, Johannes; Parthasarathy, Anutthaman; Buckel, Wolfgang
  • Journal of Biological Chemistry, Vol. 288, Issue 16
  • DOI: 10.1074/jbc.M112.444919

Formate dehydrogenase
journal, December 1990


A physiological perspective on the origin and evolution of photosynthesis
journal, November 2017

  • Martin, William F.; Bryant, Donald A.; Beatty, J. Thomas
  • FEMS Microbiology Reviews, Vol. 42, Issue 2
  • DOI: 10.1093/femsre/fux056

Studies on the Mechanism of Electron Bifurcation Catalyzed by Electron Transferring Flavoprotein (Etf) and Butyryl-CoA Dehydrogenase (Bcd) of Acidaminococcus fermentans
journal, December 2013

  • Chowdhury, Nilanjan Pal; Mowafy, Amr M.; Demmer, Julius K.
  • Journal of Biological Chemistry, Vol. 289, Issue 8
  • DOI: 10.1074/jbc.M113.521013

A novel mode of lactate metabolism in strictly anaerobic bacteria: A novel mode of lactate metabolism in anaerobes
journal, May 2014

  • Weghoff, Marie Charlotte; Bertsch, Johannes; Müller, Volker
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12493

Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes.
journal, March 1987


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

A new view of the tree of life
journal, April 2016


cooccur : Probabilistic Species Co-Occurrence Analysis in R
journal, January 2016

  • Griffith, Daniel M.; Veech, Joseph A.; Marsh, Charles J.
  • Journal of Statistical Software, Vol. 69, Issue Code Snippet 2
  • DOI: 10.18637/jss.v069.c02

Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments
journal, February 2001


Distribution and activity of anaerobic ammonium-oxidising bacteria in natural freshwater wetland soils
journal, December 2015

  • Shen, Li-dong; Wu, Hong-sheng; Gao, Zhi-qiu
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 7
  • DOI: 10.1007/s00253-015-7191-z

A Bacterial Electron-bifurcating Hydrogenase
journal, July 2012

  • Schuchmann, Kai; Müller, Volker
  • Journal of Biological Chemistry, Vol. 287, Issue 37
  • DOI: 10.1074/jbc.M112.395038

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

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Evidence for a Hexaheteromeric Methylenetetrahydrofolate Reductase in Moorella thermoacetica
journal, July 2014

  • Mock, J.; Wang, S.; Huang, H.
  • Journal of Bacteriology, Vol. 196, Issue 18
  • DOI: 10.1128/JB.01839-14

An Alternative Path for the Evolution of Biological Nitrogen Fixation
journal, January 2011


Two functionally distinct NADP + -dependent ferredoxin oxidoreductases maintain the primary redox balance of Pyrococcus furiosus
journal, July 2017

  • Nguyen, Diep M. N.; Schut, Gerrit J.; Zadvornyy, Oleg A.
  • Journal of Biological Chemistry, Vol. 292, Issue 35
  • DOI: 10.1074/jbc.M117.794172

Microbial oxidative sulfur metabolism: biochemical evidence of the membrane-bound heterodisulfide reductase-like complex of the bacterium Aquifex aeolicus
journal, June 2016

  • Boughanemi, Souhela; Lyonnet, Jordan; Infossi, Pascale
  • FEMS Microbiology Letters, Vol. 363, Issue 15
  • DOI: 10.1093/femsle/fnw156

Electron bifurcation
journal, April 2016

  • Peters, John W.; Miller, Anne-Frances; Jones, Anne K.
  • Current Opinion in Chemical Biology, Vol. 31
  • DOI: 10.1016/j.cbpa.2016.03.007

Microbialite response to an anthropogenic salinity gradient in Great Salt Lake, Utah
journal, July 2016

  • Lindsay, M. R.; Anderson, C.; Fox, N.
  • Geobiology, Vol. 15, Issue 1
  • DOI: 10.1111/gbi.12201

The Ferredoxin:NAD + Oxidoreductase (Rnf) from the Acetogen Acetobacterium woodii Requires Na + and Is Reversibly Coupled to the Membrane Potential
journal, September 2013

  • Hess, Verena; Schuchmann, Kai; Müller, Volker
  • Journal of Biological Chemistry, Vol. 288, Issue 44
  • DOI: 10.1074/jbc.M113.510255

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


Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
journal, October 2015


“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens
journal, September 2012

  • Paul, Kristina; Nonoh, James O.; Mikulski, Lena
  • Applied and Environmental Microbiology, Vol. 78, Issue 23
  • DOI: 10.1128/AEM.02193-12

H/D exchange mass spectrometry and statistical coupling analysis reveal a role for allostery in a ferredoxin-dependent bifurcating transhydrogenase catalytic cycle
journal, January 2018

  • Berry, Luke; Poudel, Saroj; Tokmina-Lukaszewska, Monika
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1862, Issue 1
  • DOI: 10.1016/j.bbagen.2017.10.002

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival
journal, September 2015

  • Greening, Chris; Biswas, Ambarish; Carere, Carlo R.
  • The ISME Journal, Vol. 10, Issue 3
  • DOI: 10.1038/ismej.2015.153

Heterotrimeric NADH-Oxidizing Methylenetetrahydrofolate Reductase from the Acetogenic Bacterium Acetobacterium woodii
journal, March 2015

  • Bertsch, Johannes; Öppinger, Christian; Hess, Verena
  • Journal of Bacteriology, Vol. 197, Issue 9
  • DOI: 10.1128/JB.00048-15

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

The deep, hot biosphere: Twenty-five years of retrospection
journal, July 2017

  • Colman, Daniel R.; Poudel, Saroj; Stamps, Blake W.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 27
  • DOI: 10.1073/pnas.1701266114

A late methanogen origin for molybdenum-dependent nitrogenase: A late methanogen origin for Mo-nitrogenase
journal, April 2011


IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Coupled Ferredoxin and Crotonyl Coenzyme A (CoA) Reduction with NADH Catalyzed by the Butyryl-CoA Dehydrogenase/Etf Complex from Clostridium kluyveri
journal, November 2007

  • Li, F.; Hinderberger, J.; Seedorf, H.
  • Journal of Bacteriology, Vol. 190, Issue 3
  • DOI: 10.1128/JB.01417-07

Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA
journal, July 2010

  • Shock, Everett L.; Holland, Melanie; Meyer-Dombard, D’Arcy
  • Geochimica et Cosmochimica Acta, Vol. 74, Issue 14
  • DOI: 10.1016/j.gca.2009.08.036

Function of reduced pyridine nucleotide-ferredoxin oxidoreductases in saccharolytic Clostridia
journal, May 1973

  • Jungermann, K.; Thauer, R. K.; Leimenstoll, G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 305, Issue 2
  • DOI: 10.1016/0005-2728(73)90175-8

Three-Dimensional Structure of Butyryl-CoA Dehydrogenase from Megasphaera elsdenii
journal, February 1995

  • Djordjevic, Snezana; Pace, Charles P.; Stankovich, Marian T.
  • Biochemistry, Vol. 34, Issue 7
  • DOI: 10.1021/bi00007a009

[FeFe] hydrogenases and their evolution: a genomic perspective
journal, March 2007


Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG
journal, April 2010

  • Mulder, David W.; Boyd, Eric S.; Sarma, Ranjana
  • Nature, Vol. 465, Issue 7295
  • DOI: 10.1038/nature08993

Geomicrobiology of Deep-Sea Hydrothermal Vents
journal, August 1985


Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria
journal, November 2007

  • Herrmann, G.; Jayamani, E.; Mai, G.
  • Journal of Bacteriology, Vol. 190, Issue 3
  • DOI: 10.1128/JB.01422-07

A novel regulatory role of the Rnf complex of Azoarcus sp. strain BH72: rnf gene clusters in Azoarcus sp. BH72
journal, December 2011


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

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


The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis
journal, August 2017


The surprising diversity of clostridial hydrogenases: a comparative genomic perspective
journal, April 2010


Clostridium acidurici Electron-Bifurcating Formate Dehydrogenase
journal, July 2013

  • Wang, Shuning; Huang, Haiyan; Kahnt, Jörg
  • Applied and Environmental Microbiology, Vol. 79, Issue 19
  • DOI: 10.1128/AEM.02015-13

New insights into the evolutionary history of biological nitrogen fixation
journal, January 2013


The rise of oxygen in Earth’s early ocean and atmosphere
journal, February 2014

  • Lyons, Timothy W.; Reinhard, Christopher T.; Planavsky, Noah J.
  • Nature, Vol. 506, Issue 7488
  • DOI: 10.1038/nature13068

Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria
journal, April 2001


Formate dehydrogenase
journal, December 1990


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

Evolution of Molybdenum Nitrogenase during the Transition from Anaerobic to Aerobic Metabolism
journal, March 2015

  • Boyd, Eric S.; Costas, Amaya M. Garcia; Hamilton, Trinity L.
  • Journal of Bacteriology, Vol. 197, Issue 9
  • DOI: 10.1128/JB.02611-14

Thermophilic archaea activate butane via alkyl-coenzyme M formation
journal, October 2016

  • Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin
  • Nature, Vol. 539, Issue 7629
  • DOI: 10.1038/nature20152

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Native metals, electron bifurcation, and CO2 reduction in early biochemical evolution
journal, June 2018

  • Sousa, Filipa L.; Preiner, Martina; Martin, William F.
  • Current Opinion in Microbiology, Vol. 43
  • DOI: 10.1016/j.mib.2017.12.010

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

Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016


Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

The universal tree of life: an update
journal, July 2015


APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


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


The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile
journal, November 2017

  • Demmer, Julius K.; Pal Chowdhury, Nilanjan; Selmer, Thorsten
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-01746-3

Bacterial lactate dehydrogenases.
journal, January 1980


Works referencing / citing this record:

Combinatorial assembly of ferredoxin‐linked modules in Escherichia coli yields a testing platform for Rnf‐complexes
journal, May 2019

  • Schiffels, Johannes; Selmer, Thorsten
  • Biotechnology and Bioengineering, Vol. 116, Issue 9
  • DOI: 10.1002/bit.27079

Bioenergetic constraints on the origin of autotrophic metabolism
journal, January 2020

  • Boyd, Eric S.; Amenabar, Maximiliano J.; Poudel, Saroj
  • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 378, Issue 2165
  • DOI: 10.1098/rsta.2019.0151

A diverse uncultivated microbial community is responsible for organic matter degradation in the Black Sea sulphidic zone
journal, January 2020

  • Suominen, Saara; Dombrowski, Nina; Sinninghe Damsté, Jaap S.
  • Environmental Microbiology
  • DOI: 10.1111/1462-2920.14902

Electron bifurcation: progress and grand challenges
journal, January 2019

  • Yuly, Jonathon L.; Lubner, Carolyn E.; Zhang, Peng
  • Chemical Communications, Vol. 55, Issue 79
  • DOI: 10.1039/c9cc05611d

Environmental boundary conditions for the origin of life converge to an organo-sulfur metabolism
journal, November 2019

  • Goldford, Joshua E.; Hartman, Hyman; Marsland, Robert
  • Nature Ecology & Evolution, Vol. 3, Issue 12
  • DOI: 10.1038/s41559-019-1018-8