Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes

Poudel, Saroj; Dunham, Eric C.; Lindsay, Melody R.; Amenabar, Maximiliano J.; Fones, Elizabeth M.; Colman, Daniel R.; Boyd, Eric S.

doi:10.3389/fmicb.2018.01762

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

Journal Article · 03 August 2018 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2018.01762 · OSTI ID:1462762

Poudel, Saroj ^[1]; Dunham, Eric C. ^[1]; Lindsay, Melody R. ^[1]; Amenabar, Maximiliano J. ^[1]; Fones, Elizabeth M. ^[1]; Colman, Daniel R. ^[1]; Boyd, Eric S. ^[1]

Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology and Immunology

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.

View Journal Article

Cite

Export

Save

Research Organization:: Montana State Univ., Bozeman, MT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE

Grant/Contract Number:: SC0012518

OSTI ID:: 1462762

Alternate ID(s):: OSTI ID: 1510454

Journal Information:: Frontiers in Microbiology, Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (161)

Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review Buckel, Wolfgang; Thauer, Rudolf K. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00401	journal	March 2018
Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes Biegel, Eva; Schmidt, Silke; González, José M. Cellular and Molecular Life Sciences, Vol. 68, Issue 4 https://doi.org/10.1007/s00018-010-0555-8	journal	November 2010
Mechanistic insights into energy conservation by flavin-based electron bifurcation Lubner, Carolyn E.; Jennings, David P.; Mulder, David W. Nature Chemical Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nchembio.2348	journal	April 2017
Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis Sorokin, Dimitry Y.; Makarova, Kira S.; Abbas, Ben Nature Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nmicrobiol.2017.81	journal	May 2017
The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth Edwards, Katrina J.; Becker, Keir; Colwell, Frederick Annual Review of Earth and Planetary Sciences, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-earth-042711-105500	journal	May 2012
The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor Schut, Gerrit J.; Zadvornyy, Oleg; Wu, Chang-Hao Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 7 https://doi.org/10.1016/j.bbabio.2016.01.010	journal	July 2016
Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments D’Hondt, Steven; Inagaki, Fumio; Zarikian, Carlos Alvarez Nature Geoscience, Vol. 8, Issue 4 https://doi.org/10.1038/ngeo2387	journal	March 2015
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds Poudel, Saroj; Colman, Daniel R.; Fixen, Kathryn R. Journal of Bacteriology, Vol. 200, Issue 10 https://doi.org/10.1128/JB.00757-17	journal	February 2018
VhuD Facilitates Electron Flow from H2 or Formate to Heterodisulfide Reductase in Methanococcus maripaludis Costa, K. C.; Lie, T. J.; Xia, Q. Journal of Bacteriology, Vol. 195, Issue 22 https://doi.org/10.1128/JB.00895-13	journal	September 2013
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
Hydrothermal vents and the origin of life Martin, William; Baross, John; Kelley, Deborah Nature Reviews Microbiology, Vol. 6, Issue 11 https://doi.org/10.1038/nrmicro1991	journal	September 2008
Hydrogen Metabolism and the Evolution of Biological Respiration: Two separate families of enzymes that oxidize hydrogen and also produce it arose through convergent evolution Schut, Gerrit J.; Peters, John W.; Boyd, Eric S. Microbe Magazine, Vol. 9, Issue 9 https://doi.org/10.1128/microbe.9.361.1	journal	September 2014
Unification of [FeFe]-hydrogenases into three structural and functional groups Poudel, Saroj; Tokmina-Lukaszewska, Monika; Colman, Daniel R. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1860, Issue 9 https://doi.org/10.1016/j.bbagen.2016.05.034	journal	September 2016
On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation–reduction reactions Peters, John W.; Beratan, David N.; Schut, Gerrit J. Chemical Communications, Vol. 54, Issue 33 https://doi.org/10.1039/c8cc01530a	journal	January 2018
Classification and phylogeny of hydrogenases Vignais, Paulette M.; Billoud, Bernard; Meyer, Jacques FEMS Microbiology Reviews, Vol. 25, Issue 4, p. 455-501 https://doi.org/10.1111/j.1574-6976.2001.tb00587.x	journal	August 2001
Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase Costa, K. C.; Wong, P. M.; Wang, T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 24 https://doi.org/10.1073/pnas.1003653107	journal	June 2010
Defining Electron Bifurcation in the Electron-Transferring Flavoprotein Family Garcia Costas, Amaya M.; Poudel, Saroj; Miller, Anne-Frances Journal of Bacteriology, Vol. 199, Issue 21 https://doi.org/10.1128/JB.00440-17	journal	August 2017
The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications Schut, Gerrit J.; Boyd, Eric S.; Peters, John W. FEMS Microbiology Reviews, Vol. 37, Issue 2 https://doi.org/10.1111/j.1574-6976.2012.00346.x	journal	March 2013
The physiology and habitat of the last universal common ancestor Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.116	journal	July 2016
Electron Bifurcation: A Long-Hidden Energy-Coupling Mechanism Müller, Volker; Chowdhury, Nilanjan Pal; Basen, Mirko Annual Review of Microbiology, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-micro-090816-093440	journal	September 2018
On the Natural History of Flavin-Based Electron Bifurcation Baymann, Frauke; Schoepp-Cothenet, Barbara; Duval, Simon Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01357	journal	July 2018
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Insights into Flavin-based Electron Bifurcation via the NADH-dependent Reduced Ferredoxin:NADP Oxidoreductase Structure Demmer, Julius K.; Huang, Haiyan; Wang, Shuning Journal of Biological Chemistry, Vol. 290, Issue 36 https://doi.org/10.1074/jbc.M115.656520	journal	July 2015
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Peters, J. W. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1853	journal	December 1998
The fixABCX Genes in Rhodospirillum rubrum Encode a Putative Membrane Complex Participating in Electron Transfer to Nitrogenase Edgren, T.; Nordlund, S. Journal of Bacteriology, Vol. 186, Issue 7 https://doi.org/10.1128/JB.186.7.2052-2060.2004	journal	March 2004
An Electron-bifurcating Caffeyl-CoA Reductase Bertsch, Johannes; Parthasarathy, Anutthaman; Buckel, Wolfgang Journal of Biological Chemistry, Vol. 288, Issue 16 https://doi.org/10.1074/jbc.M112.444919	journal	March 2013
A physiological perspective on the origin and evolution of photosynthesis Martin, William F.; Bryant, Donald A.; Beatty, J. Thomas FEMS Microbiology Reviews, Vol. 42, Issue 2 https://doi.org/10.1093/femsre/fux056	journal	November 2017
Studies on the Mechanism of Electron Bifurcation Catalyzed by Electron Transferring Flavoprotein (Etf) and Butyryl-CoA Dehydrogenase (Bcd) of Acidaminococcus fermentans Chowdhury, Nilanjan Pal; Mowafy, Amr M.; Demmer, Julius K. Journal of Biological Chemistry, Vol. 289, Issue 8 https://doi.org/10.1074/jbc.M113.521013	journal	December 2013
A novel mode of lactate metabolism in strictly anaerobic bacteria: A novel mode of lactate metabolism in anaerobes Weghoff, Marie Charlotte; Bertsch, Johannes; Müller, Volker Environmental Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/1462-2920.12493	journal	May 2014
Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. Earl, C. D.; Ronson, C. W.; Ausubel, F. M. Journal of Bacteriology, Vol. 169, Issue 3 https://doi.org/10.1128/jb.169.3.1127-1136.1987	journal	March 1987
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
cooccur : Probabilistic Species Co-Occurrence Analysis in R Griffith, Daniel M.; Veech, Joseph A.; Marsh, Charles J. Journal of Statistical Software, Vol. 69, Issue Code Snippet 2 https://doi.org/10.18637/jss.v069.c02	journal	January 2016
Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments Stein, Lisa Y.; La Duc, Myron T.; Grundl, Timothy J. Environmental Microbiology, Vol. 3, Issue 1 https://doi.org/10.1046/j.1462-2920.2001.00154.x	journal	February 2001
Distribution and activity of anaerobic ammonium-oxidising bacteria in natural freshwater wetland soils Shen, Li-dong; Wu, Hong-sheng; Gao, Zhi-qiu Applied Microbiology and Biotechnology, Vol. 100, Issue 7 https://doi.org/10.1007/s00253-015-7191-z	journal	December 2015
A Bacterial Electron-bifurcating Hydrogenase Schuchmann, Kai; Müller, Volker Journal of Biological Chemistry, Vol. 287, Issue 37 https://doi.org/10.1074/jbc.M112.395038	journal	July 2012
Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea Kaster, A. -K.; Moll, J.; Parey, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1016761108	journal	January 2011
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production Schut, G. J.; Adams, M. W. W. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01582-08	journal	May 2009
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Evidence for a Hexaheteromeric Methylenetetrahydrofolate Reductase in Moorella thermoacetica Mock, J.; Wang, S.; Huang, H. Journal of Bacteriology, Vol. 196, Issue 18 https://doi.org/10.1128/JB.01839-14	journal	July 2014
An Alternative Path for the Evolution of Biological Nitrogen Fixation Boyd, Eric S.; Hamilton, Trinity L.; Peters, John W. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00205	journal	January 2011
NADP-Specific Electron-Bifurcating [FeFe]-Hydrogenase in a Functional Complex with Formate Dehydrogenase in Clostridium autoethanogenum Grown on CO Wang, S.; Huang, H.; Kahnt, J. Journal of Bacteriology, Vol. 195, Issue 19 https://doi.org/10.1128/JB.00678-13	journal	July 2013
Two functionally distinct NADP ⁺ -dependent ferredoxin oxidoreductases maintain the primary redox balance of Pyrococcus furiosus Nguyen, Diep M. N.; Schut, Gerrit J.; Zadvornyy, Oleg A. Journal of Biological Chemistry, Vol. 292, Issue 35 https://doi.org/10.1074/jbc.M117.794172	journal	July 2017
Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys: Cultivation of soil bacteria Sait, Michelle; Hugenholtz, Philip; Janssen, Peter H. Environmental Microbiology, Vol. 4, Issue 11 https://doi.org/10.1046/j.1462-2920.2002.00352.x	journal	November 2002
Microbial oxidative sulfur metabolism: biochemical evidence of the membrane-bound heterodisulfide reductase-like complex of the bacterium Aquifex aeolicus Boughanemi, Souhela; Lyonnet, Jordan; Infossi, Pascale FEMS Microbiology Letters, Vol. 363, Issue 15 https://doi.org/10.1093/femsle/fnw156	journal	June 2016
Electron bifurcation Peters, John W.; Miller, Anne-Frances; Jones, Anne K. Current Opinion in Chemical Biology, Vol. 31 https://doi.org/10.1016/j.cbpa.2016.03.007	journal	April 2016
Microbialite response to an anthropogenic salinity gradient in Great Salt Lake, Utah Lindsay, M. R.; Anderson, C.; Fox, N. Geobiology, Vol. 15, Issue 1 https://doi.org/10.1111/gbi.12201	journal	July 2016
Hydrogen, metals, bifurcating electrons, and proton gradients: The early evolution of biological energy conservation Martin, William F. FEBS Letters, Vol. 586, Issue 5 https://doi.org/10.1016/j.febslet.2011.09.031	journal	October 2011
The Ferredoxin:NAD ⁺ Oxidoreductase (Rnf) from the Acetogen Acetobacterium woodii Requires Na ⁺ and Is Reversibly Coupled to the Membrane Potential Hess, Verena; Schuchmann, Kai; Müller, Volker Journal of Biological Chemistry, Vol. 288, Issue 44 https://doi.org/10.1074/jbc.M113.510255	journal	September 2013
Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling Buckel, Wolfgang; Thauer, Rudolf K. Chemical Reviews, Vol. 118, Issue 7 https://doi.org/10.1021/acs.chemrev.7b00707	journal	February 2018
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics Evans, P. N.; Parks, D. H.; Chadwick, G. L. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac7745	journal	October 2015
A thermophilic bacterial origin and subsequent constraints by redox, light and salinity on the evolution of the microbial mercuric reductase: The natural history of the mercuric reductase Barkay, Tamar; Kritee, K.; Boyd, Eric Environmental Microbiology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1462-2920.2010.02260.x	journal	November 2010
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens Paul, Kristina; Nonoh, James O.; Mikulski, Lena Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/AEM.02193-12	journal	September 2012
H/D exchange mass spectrometry and statistical coupling analysis reveal a role for allostery in a ferredoxin-dependent bifurcating transhydrogenase catalytic cycle Berry, Luke; Poudel, Saroj; Tokmina-Lukaszewska, Monika Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1862, Issue 1 https://doi.org/10.1016/j.bbagen.2017.10.002	journal	January 2018
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival Greening, Chris; Biswas, Ambarish; Carere, Carlo R. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.153	journal	September 2015
Heterotrimeric NADH-Oxidizing Methylenetetrahydrofolate Reductase from the Acetogenic Bacterium Acetobacterium woodii Bertsch, Johannes; Öppinger, Christian; Hess, Verena Journal of Bacteriology, Vol. 197, Issue 9 https://doi.org/10.1128/JB.00048-15	journal	March 2015
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 Tamura, K.; Dudley, J.; Nei, M. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm092	journal	April 2007
The deep, hot biosphere: Twenty-five years of retrospection Colman, Daniel R.; Poudel, Saroj; Stamps, Blake W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1701266114	journal	July 2017
A Ferredoxin- and F ₄₂₀ H ₂ -Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea Yan, Zhen; Wang, Mingyu; Ferry, James G. mBio, Vol. 8, Issue 1 https://doi.org/10.1128/mBio.02285-16	journal	February 2017
A late methanogen origin for molybdenum-dependent nitrogenase: A late methanogen origin for Mo-nitrogenase Boyd, E. S.; Anbar, A. D.; Miller, S. Geobiology, Vol. 9, Issue 3 https://doi.org/10.1111/j.1472-4669.2011.00278.x	journal	April 2011
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
Coupled Ferredoxin and Crotonyl Coenzyme A (CoA) Reduction with NADH Catalyzed by the Butyryl-CoA Dehydrogenase/Etf Complex from Clostridium kluyveri Li, F.; Hinderberger, J.; Seedorf, H. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01417-07	journal	November 2007
Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA Shock, Everett L.; Holland, Melanie; Meyer-Dombard, D’Arcy Geochimica et Cosmochimica Acta, Vol. 74, Issue 14 https://doi.org/10.1016/j.gca.2009.08.036	journal	July 2010
Function of reduced pyridine nucleotide-ferredoxin oxidoreductases in saccharolytic Clostridia Jungermann, K.; Thauer, R. K.; Leimenstoll, G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 305, Issue 2 https://doi.org/10.1016/0005-2728(73)90175-8	journal	May 1973
Three-Dimensional Structure of Butyryl-CoA Dehydrogenase from Megasphaera elsdenii Djordjevic, Snezana; Pace, Charles P.; Stankovich, Marian T. Biochemistry, Vol. 34, Issue 7 https://doi.org/10.1021/bi00007a009	journal	February 1995
[FeFe] hydrogenases and their evolution: a genomic perspective Meyer, J. Cellular and Molecular Life Sciences, Vol. 64, Issue 9, p. 1063-1084 https://doi.org/10.1007/s00018-007-6477-4	journal	March 2007
Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG Mulder, David W.; Boyd, Eric S.; Sarma, Ranjana Nature, Vol. 465, Issue 7295 https://doi.org/10.1038/nature08993	journal	April 2010
Geomicrobiology of Deep-Sea Hydrothermal Vents Jannasch, H. W.; Mottl, M. J. Science, Vol. 229, Issue 4715 https://doi.org/10.1126/science.229.4715.717	journal	August 1985
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria Herrmann, G.; Jayamani, E.; Mai, G. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01422-07	journal	November 2007
A novel regulatory role of the Rnf complex of Azoarcus sp. strain BH72: rnf gene clusters in Azoarcus sp. BH72 Sarkar, Abhijit; Köhler, Jörg; Hurek, Thomas Molecular Microbiology, Vol. 83, Issue 2 https://doi.org/10.1111/j.1365-2958.2011.07940.x	journal	December 2011
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Methanogenesis by Methanosarcina acetivorans involves two structurally and functionally distinct classes of heterodisulfide reductase Buan, Nicole R.; Metcalf, William W. Molecular Microbiology, Vol. 75, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06990.x	journal	February 2010
The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis Ledbetter, Rhesa N.; Garcia Costas, Amaya M.; Lubner, Carolyn E. Biochemistry, Vol. 56, Issue 32 https://doi.org/10.1021/acs.biochem.7b00389	journal	August 2017
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective Calusinska, M.; Happe, T.; Joris, B. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.032771-0	journal	April 2010
Clostridium acidurici Electron-Bifurcating Formate Dehydrogenase Wang, Shuning; Huang, Haiyan; Kahnt, Jörg Applied and Environmental Microbiology, Vol. 79, Issue 19 https://doi.org/10.1128/AEM.02015-13	journal	July 2013
New insights into the evolutionary history of biological nitrogen fixation Boyd, Eric S.; Peters, John W. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00201	journal	January 2013
The rise of oxygen in Earth’s early ocean and atmosphere Lyons, Timothy W.; Reinhard, Christopher T.; Planavsky, Noah J. Nature, Vol. 506, Issue 7488 https://doi.org/10.1038/nature13068	journal	February 2014
Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria Amend, Jan P.; Shock, Everett L. FEMS Microbiology Reviews, Vol. 25, Issue 2 https://doi.org/10.1111/j.1574-6976.2001.tb00576.x	journal	April 2001
Formate dehydrogenase Ferry, James G. FEMS Microbiology Letters, Vol. 87, Issue 3-4 https://doi.org/10.1111/j.1574-6968.1990.tb04940.x	journal	December 1990
Redox bifurcations: Mechanisms and importance to life now, and at its origin: A widespread means of energy conversion in biology unfolds… Nitschke, Wolfgang; Russell, Michael J. BioEssays, Vol. 34, Issue 2 https://doi.org/10.1002/bies.201100134	journal	November 2011
Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation Buckel, Wolfgang; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.07.002	journal	February 2013
Evolution of Molybdenum Nitrogenase during the Transition from Anaerobic to Aerobic Metabolism Boyd, Eric S.; Costas, Amaya M. Garcia; Hamilton, Trinity L. Journal of Bacteriology, Vol. 197, Issue 9 https://doi.org/10.1128/JB.02611-14	journal	March 2015
Thermophilic archaea activate butane via alkyl-coenzyme M formation Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin Nature, Vol. 539, Issue 7629 https://doi.org/10.1038/nature20152	journal	October 2016
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Native metals, electron bifurcation, and CO2 reduction in early biochemical evolution Sousa, Filipa L.; Preiner, Martina; Martin, William F. Current Opinion in Microbiology, Vol. 43 https://doi.org/10.1016/j.mib.2017.12.010	journal	June 2018
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H. Nature Microbiology, Vol. 1, Issue 12 https://doi.org/10.1038/nmicrobiol.2016.170	journal	October 2016
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
NADP+ Reduction with Reduced Ferredoxin and NADP+ Reduction with NADH Are Coupled via an Electron-Bifurcating Enzyme Complex in Clostridium kluyveri Wang, S.; Huang, H.; Moll, J. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00612-10	journal	July 2010
The universal tree of life: an update Forterre, Patrick Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00717	journal	July 2015
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H ₂ Storage Thauer, Rudolf K.; Kaster, Anne-Kristin; Goenrich, Meike Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev.biochem.030508.152103	journal	June 2010
The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile Demmer, Julius K.; Pal Chowdhury, Nilanjan; Selmer, Thorsten Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01746-3	journal	November 2017
Bacterial lactate dehydrogenases. Garvie, E. I. Microbiological Reviews, Vol. 44, Issue 1 https://doi.org/10.1128/MMBR.44.1.106-139.1980	journal	January 1980
Formate dehydrogenase Ferry, J. FEMS Microbiology Letters, Vol. 87, Issue 3-4 https://doi.org/10.1016/0378-1097(90)90482-6	journal	December 1990
Potential application in amoxicillin removal of Alcaligenes sp. MMA and enzymatic studies through molecular docking Sodhi, Kushneet Kaur; Kumar, Mohit; Singh, Dileep Kumar Archives of Microbiology, Vol. 202, Issue 6 https://doi.org/10.1007/s00203-020-01868-1	journal	March 2020
Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula Roggero, Paola; Liotto, Nadia; Pozzi, Chiara Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16582-1	journal	June 2020
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
Diversity of Sea Star-Associated Densoviruses and Transcribed Endogenous Viral Elements of Densovirus Origin Jackson, Elliot W.; Wilhelm, Roland C.; Johnson, Mitchell R. Journal of Virology, Vol. 95, Issue 1 https://doi.org/10.1128/jvi.01594-20	journal	December 2020
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
Redox bifurcations: Mechanisms and importance to life now, and at its origin: A widespread means of energy conversion in biology unfolds… Nitschke, Wolfgang; Russell, Michael J. BioEssays, Vol. 34, Issue 2 https://doi.org/10.1002/bies.201100134	journal	November 2011
[FeFe] hydrogenases and their evolution: a genomic perspective Meyer, J. Cellular and Molecular Life Sciences, Vol. 64, Issue 9, p. 1063-1084 https://doi.org/10.1007/s00018-007-6477-4	journal	March 2007
Distribution and activity of anaerobic ammonium-oxidising bacteria in natural freshwater wetland soils Shen, Li-dong; Wu, Hong-sheng; Gao, Zhi-qiu Applied Microbiology and Biotechnology, Vol. 100, Issue 7 https://doi.org/10.1007/s00253-015-7191-z	journal	December 2015
Evaluating the effects of causes of death on postmortem interval estimation by ATR-FTIR spectroscopy Zhang, Kai; Wang, Qi; Liu, Ruina International Journal of Legal Medicine, Vol. 134, Issue 2 https://doi.org/10.1007/s00414-019-02042-z	journal	March 2019
Function of reduced pyridine nucleotide-ferredoxin oxidoreductases in saccharolytic Clostridia Jungermann, K.; Thauer, R. K.; Leimenstoll, G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 305, Issue 2 https://doi.org/10.1016/0005-2728(73)90175-8	journal	May 1973
Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation Buckel, Wolfgang; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.07.002	journal	February 2013
The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor Schut, Gerrit J.; Zadvornyy, Oleg; Wu, Chang-Hao Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 7 https://doi.org/10.1016/j.bbabio.2016.01.010	journal	July 2016
Unification of [FeFe]-hydrogenases into three structural and functional groups Poudel, Saroj; Tokmina-Lukaszewska, Monika; Colman, Daniel R. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1860, Issue 9 https://doi.org/10.1016/j.bbagen.2016.05.034	journal	September 2016
H/D exchange mass spectrometry and statistical coupling analysis reveal a role for allostery in a ferredoxin-dependent bifurcating transhydrogenase catalytic cycle Berry, Luke; Poudel, Saroj; Tokmina-Lukaszewska, Monika Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1862, Issue 1 https://doi.org/10.1016/j.bbagen.2017.10.002	journal	January 2018
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
Hydrogen, metals, bifurcating electrons, and proton gradients: The early evolution of biological energy conservation Martin, William F. FEBS Letters, Vol. 586, Issue 5 https://doi.org/10.1016/j.febslet.2011.09.031	journal	October 2011
Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA Shock, Everett L.; Holland, Melanie; Meyer-Dombard, D’Arcy Geochimica et Cosmochimica Acta, Vol. 74, Issue 14 https://doi.org/10.1016/j.gca.2009.08.036	journal	July 2010
The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis Ledbetter, Rhesa N.; Garcia Costas, Amaya M.; Lubner, Carolyn E. Biochemistry, Vol. 56, Issue 32 https://doi.org/10.1021/acs.biochem.7b00389	journal	August 2017
Three-Dimensional Structure of Butyryl-CoA Dehydrogenase from Megasphaera elsdenii Djordjevic, Snezana; Pace, Charles P.; Stankovich, Marian T. Biochemistry, Vol. 34, Issue 7 https://doi.org/10.1021/bi00007a009	journal	February 1995
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival Greening, Chris; Biswas, Ambarish; Carere, Carlo R. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.153	journal	September 2015
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG Mulder, David W.; Boyd, Eric S.; Sarma, Ranjana Nature, Vol. 465, Issue 7295 https://doi.org/10.1038/nature08993	journal	April 2010
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
The rise of oxygen in Earth’s early ocean and atmosphere Lyons, Timothy W.; Reinhard, Christopher T.; Planavsky, Noah J. Nature, Vol. 506, Issue 7488 https://doi.org/10.1038/nature13068	journal	February 2014
Mechanistic insights into energy conservation by flavin-based electron bifurcation Lubner, Carolyn E.; Jennings, David P.; Mulder, David W. Nature Chemical Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nchembio.2348	journal	April 2017
Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments D’Hondt, Steven; Inagaki, Fumio; Zarikian, Carlos Alvarez Nature Geoscience, Vol. 8, Issue 4 https://doi.org/10.1038/ngeo2387	journal	March 2015
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H. Nature Microbiology, Vol. 1, Issue 12 https://doi.org/10.1038/nmicrobiol.2016.170	journal	October 2016
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Hydrothermal vents and the origin of life Martin, William; Baross, John; Kelley, Deborah Nature Reviews Microbiology, Vol. 6, Issue 11 https://doi.org/10.1038/nrmicro1991	journal	September 2008
The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile Demmer, Julius K.; Pal Chowdhury, Nilanjan; Selmer, Thorsten Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01746-3	journal	November 2017
Rhizosphere bacteriome structure and functions Ling, Ning; Wang, Tingting; Kuzyakov, Yakov Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28448-9	journal	February 2022
Mating pair stabilization mediates bacterial conjugation species specificity Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C. Nature Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/s41564-022-01146-4	journal	June 2022
Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans Androsiuk, Piotr; Okorski, Adam; Paukszto, Łukasz Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-05428-z	journal	February 2022
On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation–reduction reactions Peters, John W.; Beratan, David N.; Schut, Gerrit J. Chemical Communications, Vol. 54, Issue 33 https://doi.org/10.1039/c8cc01530a	journal	January 2018
Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments Stein, Lisa Y.; La Duc, Myron T.; Grundl, Timothy J. Environmental Microbiology, Vol. 3, Issue 1 https://doi.org/10.1046/j.1462-2920.2001.00154.x	journal	February 2001
Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys: Cultivation of soil bacteria Sait, Michelle; Hugenholtz, Philip; Janssen, Peter H. Environmental Microbiology, Vol. 4, Issue 11 https://doi.org/10.1046/j.1462-2920.2002.00352.x	journal	November 2002
Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase Costa, K. C.; Wong, P. M.; Wang, T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 24 https://doi.org/10.1073/pnas.1003653107	journal	June 2010
The deep, hot biosphere: Twenty-five years of retrospection Colman, Daniel R.; Poudel, Saroj; Stamps, Blake W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1701266114	journal	July 2017
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 Tamura, K.; Dudley, J.; Nei, M. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm092	journal	April 2007
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective Calusinska, M.; Happe, T.; Joris, B. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.032771-0	journal	April 2010
Microbialite response to an anthropogenic salinity gradient in Great Salt Lake, Utah Lindsay, M. R.; Anderson, C.; Fox, N. Geobiology, Vol. 15, Issue 1 https://doi.org/10.1111/gbi.12201	journal	July 2016
Methanogenesis by Methanosarcina acetivorans involves two structurally and functionally distinct classes of heterodisulfide reductase Buan, Nicole R.; Metcalf, William W. Molecular Microbiology, Vol. 75, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06990.x	journal	February 2010
The Heterodisulfide Reductase from Methanobacterium Thermoautotrophicum Contains Sequence Motifs Characteristic of pyridine-Nucleotide-Dependent Thioredoxin Reductases Hedderich, Reiner; Koch, Jurgen; Linder, Dietmar European Journal of Biochemistry, Vol. 225, Issue 1 https://doi.org/10.1111/j.1432-1033.1994.00253.x	journal	October 1994
A late methanogen origin for molybdenum-dependent nitrogenase: A late methanogen origin for Mo-nitrogenase Boyd, E. S.; Anbar, A. D.; Miller, S. Geobiology, Vol. 9, Issue 3 https://doi.org/10.1111/j.1472-4669.2011.00278.x	journal	April 2011
Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria Amend, Jan P.; Shock, Everett L. FEMS Microbiology Reviews, Vol. 25, Issue 2 https://doi.org/10.1111/j.1574-6976.2001.tb00576.x	journal	April 2001
The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications Schut, Gerrit J.; Boyd, Eric S.; Peters, John W. FEMS Microbiology Reviews, Vol. 37, Issue 2 https://doi.org/10.1111/j.1574-6976.2012.00346.x	journal	March 2013
Geomicrobiology of Deep-Sea Hydrothermal Vents Jannasch, H. W.; Mottl, M. J. Science, Vol. 229, Issue 4715 https://doi.org/10.1126/science.229.4715.717	journal	August 1985
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Peters, J. W. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1853	journal	December 1998
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics Evans, P. N.; Parks, D. H.; Chadwick, G. L. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac7745	journal	October 2015
Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. Earl, C. D.; Ronson, C. W.; Ausubel, F. M. Journal of Bacteriology, Vol. 169, Issue 3 https://doi.org/10.1128/jb.169.3.1127-1136.1987	journal	March 1987
Hydrogen Metabolism and the Evolution of Biological Respiration: Two separate families of enzymes that oxidize hydrogen and also produce it arose through convergent evolution Schut, Gerrit J.; Peters, John W.; Boyd, Eric S. Microbe Magazine, Vol. 9, Issue 9 https://doi.org/10.1128/microbe.9.361.1	journal	September 2014
The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth Edwards, Katrina J.; Becker, Keir; Colwell, Frederick Annual Review of Earth and Planetary Sciences, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-earth-042711-105500	journal	May 2012
Electron Bifurcation: A Long-Hidden Energy-Coupling Mechanism Müller, Volker; Chowdhury, Nilanjan Pal; Basen, Mirko Annual Review of Microbiology, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-micro-090816-093440	journal	September 2018
Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H ₂ Storage Thauer, Rudolf K.; Kaster, Anne-Kristin; Goenrich, Meike Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev.biochem.030508.152103	journal	June 2010
cooccur : Probabilistic Species Co-Occurrence Analysis in R Griffith, Daniel M.; Veech, Joseph A.; Marsh, Charles J. Journal of Statistical Software, Vol. 69, Issue Code Snippet 2 https://doi.org/10.18637/jss.v069.c02	journal	January 2016
New insights into the evolutionary history of biological nitrogen fixation Boyd, Eric S.; Peters, John W. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00201	journal	January 2013
Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review Buckel, Wolfgang; Thauer, Rudolf K. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00401	journal	March 2018
On the Natural History of Flavin-Based Electron Bifurcation Baymann, Frauke; Schoepp-Cothenet, Barbara; Duval, Simon Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01357	journal	July 2018

Cited By (4)

Combinatorial assembly of ferredoxin‐linked modules in Escherichia coli yields a testing platform for Rnf‐complexes Schiffels, Johannes; Selmer, Thorsten Biotechnology and Bioengineering, Vol. 116, Issue 9 https://doi.org/10.1002/bit.27079	journal	May 2019
Environmental boundary conditions for the origin of life converge to an organo-sulfur metabolism Goldford, Joshua E.; Hartman, Hyman; Marsland, Robert Nature Ecology & Evolution, Vol. 3, Issue 12 https://doi.org/10.1038/s41559-019-1018-8	journal	November 2019
Bioenergetic constraints on the origin of autotrophic metabolism Boyd, Eric S.; Amenabar, Maximiliano J.; Poudel, Saroj Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 378, Issue 2165 https://doi.org/10.1098/rsta.2019.0151	journal	January 2020
A diverse uncultivated microbial community is responsible for organic matter degradation in the Black Sea sulphidic zone Suominen, Saara; Dombrowski, Nina; Sinninghe Damsté, Jaap S. Environmental Microbiology https://doi.org/10.1111/1462-2920.14902	journal	January 2020

Similar Records

The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+

Journal Article · 2019 · Journal of Biological Chemistry · OSTI ID:1769438

Schut, Gerrit J.; Mohamed-Raseek, Nishya; Tokmina-Lukaszewska, Monika; +11 more

Defining Electron Bifurcation in the Electron-Transferring Flavoprotein Family

Journal Article · 2017 · Journal of Bacteriology · OSTI ID:1469839

Garcia Costas, Amaya M.; Poudel, Saroj; Miller, Anne -Frances; +9 more

An Abundant and Diverse New Family of Electron Bifurcating Enzymes With a Non-canonical Catalytic Mechanism

Journal Article · 2022 · Frontiers in Microbiology · OSTI ID:1875316

Schut, Gerrit J.; Haja, Dominik K.; Feng, Xiang; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
electron bifurcation
flavin
ferredoxin
anoxic
subsurface
oxidoreductase
LUCA
metagenomes

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

Citation Formats

References (161)

Cited By (4)

Similar Records

Related Subjects