Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds

Poudel, Saroj; Colman, Daniel R.; Fixen, Kathryn R.; Ledbetter, Rhesa N.; Zheng, Yanning; Pence, Natasha; Seefeldt, Lance C.; Peters, John W.; Harwood, Caroline S.; Boyd, Eric S.; Metcalf, William W.

doi:10.1128/JB.00757-17

Title: Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds

Journal Article · Mon Feb 26 00:00:00 EST 2018 · Journal of Bacteriology

DOI:https://doi.org/10.1128/JB.00757-17· OSTI ID:1470211

Poudel, Saroj ^[1]; Colman, Daniel R. ^[1];

^[2]; Ledbetter, Rhesa N. ^[3]; Zheng, Yanning ^[4]; Pence, Natasha ^[5]; Seefeldt, Lance C. ^[3]; Peters, John W. ^[5];

^[4];

^[1]; Metcalf, William W. ^[6]

Montana State Univ., Bozeman, MT (United States)
Univ. of Minnesota, St. Paul, MN (United States)
Utah State Univ., Logan, UT (United States)
Univ. of Washington, Seattle, WA (United States)
Washington State Univ., Pullman, WA (United States)
Univ. of Illinois at Urbana Champaign, Urbana, IL (United States)

Nitrogenase catalyzes the reduction of dinitrogen (N₂) using low-potential electrons from ferredoxin (Fd) or flavodoxin (Fld) through an ATP-dependent process. Since its emergence in an anaerobic chemoautotroph, this oxygen (O₂)-sensitive enzyme complex has evolved to operate in a variety of genomic and metabolic backgrounds, including those of aerobes, anaerobes, chemotrophs, and phototrophs. However, whether pathways of electron delivery to nitrogenase are influenced by these different metabolic backgrounds is not well understood. Here, we report the distribution of homologs of Fds, Flds, and Fd-/Fld-reducing enzymes in 359 genomes of putative N₂ fixers (diazotrophs). Six distinct lineages of nitrogenase were identified, and their distributions largely corresponded to differences in the host cells' ability to integrate O₂ or light into energy metabolism. The predicted pathways of electron transfer to nitrogenase in aerobes, facultative anaerobes, and phototrophs varied from those in anaerobes at the levels of Fds/Flds used to reduce nitrogenase, the enzymes that generate reduced Fds/Flds, and the putative substrates of these enzymes. Proteins that putatively reduce Fd with hydrogen or pyruvate were enriched in anaerobes, while those that reduce Fd with NADH/NADPH were enriched in aerobes, facultative anaerobes, and anoxygenic phototrophs. Here, the energy metabolism of aerobic, facultatively anaerobic, and anoxygenic phototrophic diazotrophs often yields reduced NADH/NADPH that is not sufficiently reduced to drive N₂ reduction. At least two mechanisms have been acquired by these taxa to overcome this limitation and to generate electrons with potentials capable of reducing Fd. These include the bifurcation of electrons or the coupling of Fd reduction to reverse ion translocation.

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Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy)

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

Grant/Contract Number:: SC0012518

OSTI ID:: 1470211

Journal Information:: Journal of Bacteriology, Vol. 200, Issue 10; Related Information: BETCy partners with Montana State University (lead); Arizona State University; National Renewable Energy Laboratory; University of Georgia; University of Kentucky; University of Washington; Utah State University; ISSN 0021-9193

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 43 works

Citation information provided by
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References (124)

The molybdenum and vanadium nitrogenases of Azotobacter chroococcum: effect of elevated temperature on N2 reduction Dilworth, M. J.; Eldridge, M. E.; Eady, R. R. Biochemical Journal, Vol. 289, Issue 2 https://doi.org/10.1042/bj2890395	journal	January 1993
Molecular cloning and sequence analysis of the structural gene of ferredoxin I from the photosynthetic bacterium Rhodobacter capsulatus. Schatt, E.; Jouanneau, Y.; Vignais, P. M. Journal of Bacteriology, Vol. 171, Issue 11 https://doi.org/10.1128/jb.171.11.6218-6226.1989	journal	November 1989
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
Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120 Ermakova, M.; Battchikova, N.; Richaud, P. Proceedings of the National Academy of Sciences, Vol. 111, Issue 30 https://doi.org/10.1073/pnas.1407327111	journal	July 2014
Classifying the metal dependence of uncharacterized nitrogenases McGlynn, Shawn E.; Boyd, Eric S.; Peters, John W. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00419	journal	January 2013
Flavodoxin from the nitrogen-fixing cyanobacterium Anabaena PCC 7119 Fillat, Maria F.; Sandmann, Gerhard; Gomez-Moreno, Carlos Archives of Microbiology, Vol. 150, Issue 2 https://doi.org/10.1007/BF00425156	journal	June 1988
Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii. Jacobson, M. R.; Brigle, K. E.; Bennett, L. T. Journal of Bacteriology, Vol. 171, Issue 2 https://doi.org/10.1128/jb.171.2.1017-1027.1989	journal	February 1989
A pathway for biological methane production using bacterial iron-only nitrogenase Zheng, Yanning; Harris, Derek F.; Yu, Zheng Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0091-5	journal	January 2018
A [2Fe-2S] ferredoxin (FdVI) is essential for growth of the photosynthetic bacterium Rhodobacter capsulatus. Armengaud, J.; Meyer, C.; Jouanneau, Y. Journal of Bacteriology, Vol. 179, Issue 10 https://doi.org/10.1128/jb.179.10.3304-3309.1997	journal	May 1997
The base sequence of the nifF gene of Klebsiella pneumoniae and homology of the predicted amino acid sequence of its protein product to other flavodoxins Drummond, M. H. Biochemical Journal, Vol. 232, Issue 3 https://doi.org/10.1042/bj2320891	journal	December 1985
Stopped-flow kinetic studies of low potential electron carriers of the photosynthetic bacterium, Rhodobacter capsulatus: ferredoxin I and NifF Hallenbeck, Patrick C.; Gennaro, Giuseppa Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1365, Issue 3 https://doi.org/10.1016/S0005-2728(98)00096-6	journal	July 1998
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
[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
Open reading frame 5 (ORF5), encoding a ferredoxinlike protein, and nifQ are cotranscribed with nifE, nifN, nifX, and ORF4 in Rhodobacter capsulatus. Moreno-Vivian, C.; Hennecke, S.; Pühler, A. Journal of Bacteriology, Vol. 171, Issue 5 https://doi.org/10.1128/jb.171.5.2591-2598.1989	journal	May 1989
Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase Hu, Yilin; Ribbe, Markus W. Journal of Biological Chemistry, Vol. 288, Issue 19 https://doi.org/10.1074/jbc.r113.454041	journal	March 2013
Cloning, characterization, and regulation of nifF from Rhodobacter capsulatus. Gennaro, G.; Hübner, P.; Sandmeier, U. Journal of Bacteriology, Vol. 178, Issue 13 https://doi.org/10.1128/jb.178.13.3949-3952.1996	journal	July 1996
The involvement of the nif-associated ferredoxin-like genes fdxA and fdxN of Herbaspirillum seropedicae in nitrogen fixation Souza, André L. F.; Invitti, Adriana L.; Rego, Fabiane G. M. The Journal of Microbiology, Vol. 48, Issue 1 https://doi.org/10.1007/s12275-009-0077-y	journal	February 2010
Nitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp. grown under alternating light-dark cycles Stal, Lucas J.; Krumbein, Wolfgang E. Archives of Microbiology, Vol. 143, Issue 1 https://doi.org/10.1007/BF00414770	journal	October 1985
Respiratory Protection of Nitrogenase Activity in Azotobacter vinelandii—Roles of the Terminal Oxidases Poole, Robert K.; Hill, Susan Bioscience Reports, Vol. 17, Issue 3 https://doi.org/10.1023/A:1027336712748	journal	June 1997
Oxygen relations of nitrogen fixation in cyanobacteria. Fay, P. Microbiological Reviews, Vol. 56, Issue 2 https://doi.org/10.1128/MMBR.56.2.340-373.1992	journal	January 1992
The Specific Influence of Acidity on the Mechanism of Nitrogen Fixation by Azotobacter Burk, Dean; Lineweaver, Hans; Horner, C. Kenneth Journal of Bacteriology, Vol. 27, Issue 4 https://doi.org/10.1128/JB.27.4.325-340.1934	journal	January 1934
The Natural History of Nitrogen Fixation Raymond, Jason; Siefert, Janet L.; Staples, Christopher R. Molecular Biology and Evolution, Vol. 21, Issue 3 https://doi.org/10.1093/molbev/msh047	journal	March 2004
The Isolation and Characterization of a New Iron-Sulfur Protein from Photosynthetic Membranes Malkin, R.; Aparicio, P. J.; Arnon, D. I. Proceedings of the National Academy of Sciences, Vol. 71, Issue 6 https://doi.org/10.1073/pnas.71.6.2362	journal	June 1974
Crystallization and structure determination of 2.5-.ANG. resolution of the oxidized iron-sulfur [2Fe-2S] ferredoxin isolated from Anabaena 7120 Rypniewski, Wojciech R.; Breiter, Deborah R.; Benning, Matthew M. Biochemistry, Vol. 30, Issue 17 https://doi.org/10.1021/bi00231a003	journal	April 1991
The Bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 Is Reduced by Flavodoxin and Ferredoxin and Is Essential under Mixotrophic, Nitrate-limiting Conditions Gutekunst, Kirstin; Chen, Xi; Schreiber, Karoline Journal of Biological Chemistry, Vol. 289, Issue 4 https://doi.org/10.1074/jbc.M113.526376	journal	December 2013
Diversity and Activity of Alternative Nitrogenases in Sequenced Genomes and Coastal Environments McRose, Darcy L.; Zhang, Xinning; Kraepiel, Anne M. L. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00267	journal	February 2017
Transcriptional Profiling of Nitrogen Fixation in Azotobacter vinelandii Hamilton, T. L.; Ludwig, M.; Dixon, R. Journal of Bacteriology, Vol. 193, Issue 17 https://doi.org/10.1128/JB.05099-11	journal	July 2011
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
Asymmetric Dimeric Structure of Ferredoxin-NAD(P)+ Oxidoreductase from the Green Sulfur Bacterium Chlorobaculum tepidum: Implications for Binding Ferredoxin and NADP+ Muraki, Norifumi; Seo, Daisuke; Shiba, Tomoo Journal of Molecular Biology, Vol. 401, Issue 3 https://doi.org/10.1016/j.jmb.2010.06.024	journal	August 2010
Purification of the nitrogenase proteins from Clostridium pasteurianum Tso, Man-Yin W.; Ljones, Torbjørn; Burris, R. H. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 267, Issue 3 https://doi.org/10.1016/0005-2728(72)90193-4	journal	June 1972
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
Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria Anantharaman, K.; Breier, J. A.; Sheik, C. S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 1 https://doi.org/10.1073/pnas.1215340110	journal	December 2012
The heterocyst-specific fdxH gene product of the cyanobacterium Anabaena sp. PCC 7120 is important but not essential for nitrogen fixation Masepohl, B.; Schölisch, K.; Görlitz, K. Molecular and General Genetics MGG, Vol. 253, Issue 6 https://doi.org/10.1007/s004380050383	journal	February 1997
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
Nitrogen Fixation at 92 C by a Hydrothermal Vent Archaeon Mehta, M. P.; Baross, J. A. Science, Vol. 314, Issue 5806 https://doi.org/10.1126/science.1134772	journal	December 2006
Identification of Global Ferredoxin Interaction Networks in Chlamydomonas reinhardtii Peden, Erin A.; Boehm, Marko; Mulder, David W. Journal of Biological Chemistry, Vol. 288, Issue 49 https://doi.org/10.1074/jbc.M113.483727	journal	October 2013
The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5 Therien, Jesse B.; Artz, Jacob H.; Poudel, Saroj Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01305	journal	July 2017
Purification and characterization of ferredoxin–NAD(P)+ reductase from the green sulfur bacterium Chlorobium tepidum Seo, Daisuke; Sakurai, Hidehiro Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1597, Issue 1 https://doi.org/10.1016/S0167-4838(02)00269-8	journal	May 2002
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
Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase Rubio, Luis M.; Ludden, Paul W. Annual Review of Microbiology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.162737	journal	October 2008
Bacterial Alternative Nitrogen Fixation Systems Joerger, Rolf D.; Bishop, Paul E.; Evans, Harold J. CRC Critical Reviews in Microbiology, Vol. 16, Issue 1 https://doi.org/10.3109/10408418809104465	journal	January 1988
Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae. Roberts, G. P.; MacNeil, T.; MacNeil, D. Journal of Bacteriology, Vol. 136, Issue 1 https://doi.org/10.1128/JB.136.1.267-279.1978	journal	January 1978
Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Hageman, R. V.; Burris, R. H. Proceedings of the National Academy of Sciences, Vol. 75, Issue 6 https://doi.org/10.1073/pnas.75.6.2699	journal	June 1978
Molecular Biological Analysis of a Bidirectional Hydrogenase from Cyanobacteria Schmitz, Oliver; Boison, Gudrun; Hilscher, Ralf European Journal of Biochemistry, Vol. 233, Issue 1 https://doi.org/10.1111/j.1432-1033.1995.266_1.x	journal	October 1995
Mechanism of Mo-Dependent Nitrogenase Seefeldt, Lance C.; Hoffman, Brian M.; Dean, Dennis R. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.78.070907.103812	journal	June 2009
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
The Genome of Heliobacterium modesticaldum, a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus Sattley, W. M.; Madigan, M. T.; Swingley, W. D. Journal of Bacteriology, Vol. 190, Issue 13 https://doi.org/10.1128/JB.00299-08	journal	April 2008
Regulation of Uptake Hydrogenase and Effects of Hydrogen Utilization on Gene Expression in Rhodopseudomonas palustris Rey, F. E.; Oda, Y.; Harwood, C. S. Journal of Bacteriology, Vol. 188, Issue 17 https://doi.org/10.1128/JB.00381-06	journal	August 2006
The vanadium- and molybdenum-containing nitrogenases of Azotobacter chroococcum. Comparison of mid-point potentials and kinetics of reduction by sodium dithionite of the iron proteins with bound magnesium adenosine 5′-diphosphate Bergström, J.; Eady, R. R.; Thorneley, R. N. F. Biochemical Journal, Vol. 251, Issue 1 https://doi.org/10.1042/bj2510165	journal	April 1988
Complete Genomic Sequence of the Filamentous Nitrogen-fixing Cyanobacterium Anabaena sp. Strain PCC 7120 Kaneko, T. DNA Research, Vol. 8, Issue 5 https://doi.org/10.1093/dnares/8.5.205	journal	January 2001
Average oxidation state of carbon in proteins Dick, Jeffrey M. Journal of The Royal Society Interface, Vol. 11, Issue 100 https://doi.org/10.1098/rsif.2013.1095	journal	November 2014
Identification of amino acids responsible for the oxygen sensitivity of ferredoxins from Anabaena variabilis using site-directed mutagenesis Singh, B. B.; Curdt, I.; Jakobs, C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1412, Issue 3 https://doi.org/10.1016/S0005-2728(99)00069-9	journal	August 1999
Correction for creatine interference with the direct indophenol measurement of NH3 in steady-state nitrogenase assays Dilworth, Michael J.; Eldridge, Marie E.; Eady, Robert R. Analytical Biochemistry, Vol. 207, Issue 1 https://doi.org/10.1016/0003-2697(92)90491-O	journal	November 1992
Crystal structure of the nickel–iron hydrogenase from Desulfovibrio gigas Volbeda, Anne; Charon, Marie-Hélène; Piras, Claudine Nature, Vol. 373, Issue 6515 https://doi.org/10.1038/373580a0	journal	February 1995
Purification and properties of a nif-specific flavodoxin from the photosynthetic bacterium Rhodobacter capsulatus. Yakunin, A. F.; Gennaro, G.; Hallenbeck, P. C. Journal of Bacteriology, Vol. 175, Issue 21 https://doi.org/10.1128/jb.175.21.6775-6780.1993	journal	November 1993
The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB Klipp, Werner; Reil�nder, Helmut; Schl�ter, Andreas MGG Molecular & General Genetics, Vol. 216, Issue 2-3 https://doi.org/10.1007/BF00334368	journal	April 1989
The nitrogenase system from Azotobacter: two-enzyme requirement for N2 reduction, ATP-dependent H2 evolution, and ATP hydrolysis. Bulen, W. A.; LeComte, J. R. Proceedings of the National Academy of Sciences, Vol. 56, Issue 3 https://doi.org/10.1073/pnas.56.3.979	journal	September 1966
Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean Falkowski, Paul G. Nature, Vol. 387, Issue 6630 https://doi.org/10.1038/387272a0	journal	May 1997
Characterization of an fdxN mutant of Rhodobacter capsulatus indicates that ferredoxin I serves as electron donor to nitrogenase Jouanneau, Yves; Meyer, Christine; Naud, Isabelle Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1232, Issue 1-2 https://doi.org/10.1016/0005-2728(95)00106-X	journal	November 1995
Iron-sulphur clusters and the problem with oxygen Imlay, James A. Molecular Microbiology, Vol. 59, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05028.x	journal	February 2006
Roles of nifF and nifJ gene products in electron transport to nitrogenase in Klebsiella pneumoniae. Hill, S.; Kavanagh, E. P. Journal of Bacteriology, Vol. 141, Issue 2 https://doi.org/10.1128/JB.141.2.470-475.1980	journal	January 1980
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
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
The importance of flavodoxin for environmental stress tolerance in photosynthetic microorganisms and transgenic plants. Mechanism, evolution and biotechnological potential Lodeyro, Anabella F.; Ceccoli, Romina D.; Pierella Karlusich, Juan J. FEBS Letters, Vol. 586, Issue 18 https://doi.org/10.1016/j.febslet.2012.07.026	journal	July 2012
Bacterial Electron Transport Chains Anraku, Yasuhiro Annual Review of Biochemistry, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.bi.57.070188.000533	journal	June 1988
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
Physiological and isotopic characteristics of nitrogen fixation by hyperthermophilic methanogens: Key insights into nitrogen anabolism of the microbial communities in Archean hydrothermal systems Nishizawa, Manabu; Miyazaki, Junichi; Makabe, Akiko Geochimica et Cosmochimica Acta, Vol. 138 https://doi.org/10.1016/j.gca.2014.04.021	journal	August 2014
Cyanobacterial Hydrogenases and Hydrogen Metabolism Revisited: Recent Progress and Future Prospects Khanna, Namita; Lindblad, Peter International Journal of Molecular Sciences, Vol. 16, Issue 12 https://doi.org/10.3390/ijms160510537	journal	May 2015
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
Crystallization and preliminary analysis of oxidized, recombinant, heterocyst [2Fe2S] ferredoxin from Anabaena 7120 Jacobson, Bruce L.; Chae, Young Kee; Böhme, Herbert Archives of Biochemistry and Biophysics, Vol. 294, Issue 1 https://doi.org/10.1016/0003-9861(92)90169-W	journal	April 1992
Evidence That the P _i Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle Yang, Zhi-Yong; Ledbetter, Rhesa; Shaw, Sudipta Biochemistry, Vol. 55, Issue 26 https://doi.org/10.1021/acs.biochem.6b00421	journal	June 2016
Structure−Function Relationships of Alternative Nitrogenases Eady, Robert R. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950057h	journal	January 1996
A distinct ferredoxin for nitrogen fixation isolated from heterocysts of the cyanobacterium Anabaena variabilis Schrautemeier, Bernhard; Böhme, Herbert FEBS Letters, Vol. 184, Issue 2 https://doi.org/10.1016/0014-5793(85)80627-X	journal	May 1985
Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains Sandmann, Gerhard; Peleato, M. Luisa; Fillat, Maria F. Photosynthesis Research, Vol. 26, Issue 2 https://doi.org/10.1007/BF00047083	journal	November 1990
Biochemical and Crystallographic Characterization of Ferredoxin−NADP ⁺ Reductase from Nonphotosynthetic Tissues ^† ^, ^‡ Aliverti, Alessandro; Faber, Rick; Finnerty, Casey M. Biochemistry, Vol. 40, Issue 48 https://doi.org/10.1021/bi011224c	journal	December 2001
Genome Sequence of Azotobacter vinelandii, an Obligate Aerobe Specialized To Support Diverse Anaerobic Metabolic Processes Setubal, J. C.; dos Santos, P.; Goldman, B. S. Journal of Bacteriology, Vol. 191, Issue 14 https://doi.org/10.1128/JB.00504-09	journal	May 2009
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
Construction and characterization of an Azotobacter vinelandii strain with mutations in the genes encoding flavodoxin and ferredoxin I. Martin, A. E.; Burgess, B. K.; Iismaa, S. E. Journal of Bacteriology, Vol. 171, Issue 6 https://doi.org/10.1128/jb.171.6.3162-3167.1989	journal	June 1989
Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae Arnold, Walter; Rump, Andreas; Klipp, Werner Journal of Molecular Biology, Vol. 203, Issue 3 https://doi.org/10.1016/0022-2836(88)90205-7	journal	October 1988
Electron transport to nitrogenase in Klebsiella pneumoniae. Nieva-Gomez, D.; Roberts, G. P.; Klevickis, S. Proceedings of the National Academy of Sciences, Vol. 77, Issue 5 https://doi.org/10.1073/pnas.77.5.2555	journal	May 1980
Principles of Geobiochemistry Shock, Everett L.; Boyd, Eric S. Elements, Vol. 11, Issue 6 https://doi.org/10.2113/gselements.11.6.395	journal	November 2015
Purification and characterization of a fix ABCX-linked 2[4Fe-4S] ferredoxin from Azotobacter vinelandii Reyntjens, Bruno; Jollie, David R.; Stephens, Philip J. JBIC Journal of Biological Inorganic Chemistry, Vol. 2, Issue 5 https://doi.org/10.1007/s007750050174	journal	October 1997
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
A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase Simpson, F.; Burris, R. Science, Vol. 224, Issue 4653 https://doi.org/10.1126/science.6585956	journal	June 1984
CDD: NCBI's conserved domain database Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1221	journal	November 2014
Electron transfer to nitrogenase in Klebsiella pneumoniae. nifF gene cloned and the gene product, a flavodoxin, purified Deistung, J.; Cannon, F. C.; Cannon, M. C. Biochemical Journal, Vol. 231, Issue 3 https://doi.org/10.1042/bj2310743	journal	November 1985
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 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
Nucleotide Hydrolysis and Protein Conformational Changes in Azotobacter vinelandii Nitrogenase Iron Protein: Defining the Function of Aspartate 129 Lanzilotta, William N.; Ryle, Matthew J.; Seefeldt, Lance C. Biochemistry, Vol. 34, Issue 34 https://doi.org/10.1021/bi00034a003	journal	August 1995
Purification and molecular properties of a soluble ferredoxin from Rhodopseudomonas capsulata Hallenbeck, Patrick C.; Jouanneau, Yves; Vignais, Paulette M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 681, Issue 2 https://doi.org/10.1016/0005-2728(82)90020-2	journal	August 1982
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
Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus . Characterization of two membrane-bound iron-sulfur proteins Jouanneau, Yves; Jeong, Ho-Sang; Hugo, Nicolas European Journal of Biochemistry, Vol. 251, Issue 1-2 https://doi.org/10.1046/j.1432-1327.1998.2510054.x	journal	January 1998
Redox and spectroscopic properties of oxidized MoFe protein from Azotobacter vinelandii Watt, G. D.; Burns, A.; Lough, S. Biochemistry, Vol. 19, Issue 21 https://doi.org/10.1021/bi00562a035	journal	October 1980
Electron transport to nitrogenase in Rhodospirillum rubrum: Identification of a new fdxN gene encoding the primary electron donor to nitrogenase Edgren, Tomas; Nordlund, Stefan FEMS Microbiology Letters, Vol. 245, Issue 2 https://doi.org/10.1016/j.femsle.2005.03.024	journal	April 2005
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
Electron donation to nitrogenase in heterocysts of cyanobacteria Neuer, Gabriele; Bothe, Hermann Archives of Microbiology, Vol. 143, Issue 2 https://doi.org/10.1007/BF00411045	journal	November 1985
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes Dos Santos, Patricia C.; Fang, Zhong; Mason, Steven W. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-162	journal	January 2012
Identification of a new class of nitrogen fixation genes in Rhodobacter capsalatus: a putative membrane complex involved in electron transport to nitrogenase Schmehl, Manfred; Jahn, Andreas; Meyer zu Vilsendorf, Andreas MGG Molecular & General Genetics, Vol. 241-241, Issue 5-6 https://doi.org/10.1007/BF00279903	journal	December 1993
Role of a Ferredoxin Gene Cotranscribed with the nifHDK Operon in N2 Fixation and Nitrogenase "Switch-Off" of Azoarcus sp. Strain BH72 Egener, T.; Martin, D. E.; Sarkar, A. Journal of Bacteriology, Vol. 183, Issue 12 https://doi.org/10.1128/JB.183.12.3752-3760.2001	journal	June 2001
Characterization of the genome region encoding an fdxH-type ferredoxin and a new 2[4Fe-4S] ferredoxin from the nonheterocystous, nitrogen-fixing cyanobacterium Plectonema boryanum PCC 73110. Schrautemeier, B.; Cassing, A.; Böhme, H. Journal of Bacteriology, Vol. 176, Issue 4 https://doi.org/10.1128/jb.176.4.1037-1046.1994	journal	February 1994
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
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia Dekas, A. E.; Poretsky, R. S.; Orphan, V. J. Science, Vol. 326, Issue 5951 https://doi.org/10.1126/science.1178223	journal	October 2009
fixA, B and C genes are essential for symbiotic and free-living, microaerobic nitrogen fixation Gubler, Marcel; Hennecke, Hauke FEBS Letters, Vol. 200, Issue 1 https://doi.org/10.1016/0014-5793(86)80536-1	journal	May 1986
Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes Bolhuis, Henk; Severin, Ina; Confurius-Guns, Veronique The ISME Journal, Vol. 4, Issue 1 https://doi.org/10.1038/ismej.2009.99	journal	September 2009
Azotobacter vinelandii NADPH:Ferredoxin Reductase Cloning, Sequencing, and Overexpression Isas, J. Mario; Yannone, Steven M.; Burgess, Barbara K. Journal of Biological Chemistry, Vol. 270, Issue 36 https://doi.org/10.1074/jbc.270.36.21258	journal	September 1995
Characterization of the fixABC region of Azorhizobium caulinodans ORS571 and identification of a new nitrogen fixation gene Alexandre Kaminski, P.; Norel, Fran�oise; Desnoues, Nicole MGG Molecular & General Genetics, Vol. 214, Issue 3 https://doi.org/10.1007/BF00330486	journal	November 1988
Purification and characterization of pyruvate oxidoreductase from the photosynthetic bacterium Rhodobacter capsulatus Yakunin, Alexander F.; Hallenbeck, Patrick C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1409, Issue 1 https://doi.org/10.1016/S0005-2728(98)00145-5	journal	November 1998
Calculation of the Relative Chemical Stabilities of Proteins as a Function of Temperature and Redox Chemistry in a Hot Spring Dick, Jeffrey M.; Shock, Everett L. PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0022782	journal	August 2011
Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems Vitousek, Peter M.; Menge, Duncan N. L.; Reed, Sasha C. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621 https://doi.org/10.1098/rstb.2013.0119	journal	July 2013
Recombinant expression of the fdxD gene of Rhodobacter capsulatus and characterization of its product, a [2Fe-2S] ferredoxin Armengaud, J.; Meyer, C.; Jouanneau, Y. Biochemical Journal, Vol. 300, Issue 2 https://doi.org/10.1042/bj3000413	journal	June 1994
Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris Larimer, Frank W; Chain, Patrick; Hauser, Loren Nature Biotechnology, Vol. 22, Issue 1, p. 55-61 https://doi.org/10.1038/nbt923	journal	December 2003
Oxygen relations of nitrogen fixation in cyanobacteria Fay, P. Microbiological Reviews, Vol. 56, Issue 2 https://doi.org/10.1128/mr.56.2.340-373.1992	journal	June 1992
Clostridial pyruvate oxidoreductase and the pyruvate-oxidizing enzyme specific to nitrogen fixation in Klebsiella pneumoniae are similar enzymes. Wahl, R. C.; Orme-Johnson, W. H. Journal of Biological Chemistry, Vol. 262, Issue 22 https://doi.org/10.1016/S0021-9258(18)60987-1	journal	August 1987
The Oxygen Sensitivity of Spinach Ferredoxin and Other Iron-Sulfur Proteins Petering, David; Fee, James A.; Palmer, Graham Journal of Biological Chemistry, Vol. 246, Issue 3 https://doi.org/10.1016/S0021-9258(18)62463-9	journal	February 1971
Isolation and Characteristics of Flavodoxin from Nitrogen-fixing Clostridium pasteurianum Knight, E.; Hardy, R. W. F. Journal of Biological Chemistry, Vol. 241, Issue 12 https://doi.org/10.1016/S0021-9258(18)96528-2	journal	June 1966
Studies on the Chemical Nature of Clostridial Ferredoxin Lovenberg, Walter; Buchanan, Bob B.; Rabinowitz, Jesse C. Journal of Biological Chemistry, Vol. 238, Issue 12 https://doi.org/10.1016/S0021-9258(18)51805-6	journal	December 1963
Isolation, sequencing, and mutagenesis of the nifF gene encoding flavodoxin from Azotobacter vinelandii. Bennett, L. T.; Jacobson, M. R.; Dean, D. R. Journal of Biological Chemistry, Vol. 263, Issue 3 https://doi.org/10.1016/S0021-9258(19)57311-2	journal	January 1988
Electron transport to nitrogenase. Purification and characterization of pyruvate:flavodoxin oxidoreductase. The nifJ gene product. Shah, V. K.; Stacey, G.; Brill, W. J. Journal of Biological Chemistry, Vol. 258, Issue 19 https://doi.org/10.1016/S0021-9258(17)44340-7	journal	October 1983
Two Biologically Active Ferredoxins from the Aerobic Nitrogen-fixing Bacterium, Azotobacter vinelandii Yoch, Duane C.; Arnon, Daniel I. Journal of Biological Chemistry, Vol. 247, Issue 14 https://doi.org/10.1016/S0021-9258(19)45017-5	journal	July 1972
Purification and characterization of a novel dimeric ferredoxin (FdIII) from Rhodobacter capsulatus Jouanneau, Y.; Meyer, C.; Gaillard, J. Journal of Biological Chemistry, Vol. 268, Issue 14 https://doi.org/10.1016/S0021-9258(18)82245-1	journal	May 1993
A new [2Fe-2S] ferredoxin from Rhodobacter capsulatus. Coexpression with a 2[4Fe-4S] ferredoxin in Escherichia coli. Grabau, C.; Schatt, E.; Jouanneau, Y. Journal of Biological Chemistry, Vol. 266, Issue 5 https://doi.org/10.1016/S0021-9258(18)49987-5	journal	February 1991
Genetic analysis of functional differences among distinct ferredoxins in Rhodobacter capsulatus Saeki, K.; Suetsugu, Y.; Tokuda, K. Journal of Biological Chemistry, Vol. 266, Issue 20 https://doi.org/10.1016/S0021-9258(18)98778-8	journal	July 1991
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

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