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Annual Review of Microbiology

Volume 74, 2020

Iron-Only and Vanadium Nitrogenases: Fail-Safe Enzymes or Something More?

Abstract

The enzyme molybdenum nitrogenase converts atmospheric nitrogen gas to ammonia and is of critical importance for the cycling of nitrogen in the biosphere and for the sustainability of life. Alternative vanadium and iron-only nitrogenases that are homologous to molybdenum nitrogenases are also found in archaea and bacteria, but they have a different transition metal, either vanadium or iron, at their active sites. So far alternative nitrogenases have only been found in microbes that also have molybdenum nitrogenase. They are less widespread than molybdenum nitrogenase in bacteria and archaea, and they are less efficient. The presumption has been that alternative nitrogenases are fail-safe enzymes that are used in situations where molybdenum is limiting. Recent work indicates that vanadium nitrogenase may play a role in the global biological nitrogen cycle and iron-only nitrogenase may contribute products that shape microbial community interactions in nature.

Keyword(s): alternative nitrogenase, iron-only nitrogenase, nitrogen fixation, vanadium nitrogenase
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2020-09-08
2024-04-24
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Literature Cited

  1. 1. 
    Arcondéguy T, Jack R, Merrick M 2001. PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol. Mol. Biol. Rev. 65:180–105
     [Google Scholar]
  2. 2. 
    Bellenger JP, Xu Y, Zhang X, Morel FMM, Kraepiel AML 2014. Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N2-fixing bacteria in soils. Soil Biol. Biochem. 69:413–20
     [Google Scholar]
  3. 3. 
    Biegel E, Schmidt S, González JM, Müller V 2011. Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol. Life Sci. 68:4613–34
     [Google Scholar]
  4. 4. 
    Bishop PE, Jarlenski DM, Hetherington DR 1980. Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. . PNAS 77:127342–46
     [Google Scholar]
  5. 5. 
    Bishop PE, Jarlenski DM, Hetherington DR 1982. Expression of an alternative nitrogen fixation system in Azotobacter vinelandii. J. . Bacteriol 150:31244–51
     [Google Scholar]
  6. 6. 
    Bishop PE, Premakuman R, Dean DR, Jacobson MR, Chisnell JR et al. 1986. Nitrogen fixation by Azotobacter vinelandii strains having deletions in structural genes for nitrogenase. Science 232:474692–94
     [Google Scholar]
  7. 7. 
    Boyd ES, Hamilton TL, Peters JW 2011. An alternative path for the evolution of biological nitrogen fixation. Front. Microbiol. 2:205
     [Google Scholar]
  8. 8. 
    Boyd ES, Peters JW. 2013. New insights into the evolutionary history of biological nitrogen fixation. Front. Microbiol. 4:201
     [Google Scholar]
  9. 9. 
    Burén S, Jiménez-Vicente E, Echavarri-Erasun C, Rubio LM 2020. Biosynthesis of nitrogenase cofactors. Chem. Rev. 120:124921–68
     [Google Scholar]
  10. 10. 
    Burgess BK, Lowe DJ. 1996. Mechanism of molybdenum nitrogenase. Chem. Rev. 96:72983–3012
     [Google Scholar]
  11. 11. 
    Cherkasov N, Ibhadon AO, Fitzpatrick P 2015. A review of the existing and alternative methods for greener nitrogen fixation. Chem. Eng. Process. Process Intensif. 90:24–33
     [Google Scholar]
  12. 12. 
    Chisnell JR, Premakumar R, Bishop PE 1988. Purification of a second alternative nitrogenase from a nifHDK deletion strain of Azotobacter vinelandii. J. . Bacteriol 170:127–33
     [Google Scholar]
  13. 13. 
    Curatti L, Hernandez A, Igarashi RY, Soboh B, Zhao D, Rubio LM 2007. In vitro synthesis of the iron-molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum, and homocitrate using purified proteins. PNAS 104:4517626–31
     [Google Scholar]
  14. 14. 
    Curatti L, Ludden PW, Rubio LM 2006. NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. PNAS 103:145297–301
     [Google Scholar]
  15. 15. 
    Darnajoux R, Magain N, Renaudin M, Lutzoni F, Bellenger J-P, Zhang X 2019. Molybdenum threshold for ecosystem scale alternative vanadium nitrogenase activity in boreal forests. PNAS 116:4924682–88
     [Google Scholar]
  16. 16. 
    Demtröder L, Narberhaus F, Masepohl B 2019. Coordinated regulation of nitrogen fixation and molybdate transport by molybdenum. Mol. Microbiol. 111:117–30
     [Google Scholar]
  17. 17. 
    Demtröder L, Pfänder Y, Schäkermann S, Bandow JE, Masepohl B 2019. NifA is the master regulator of both nitrogenase systems in Rhodobacter capsulatus. . MicrobiologyOpen 8:12e921
     [Google Scholar]
  18. 18. 
    Dilworth MJ. 1966. Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochim. Biophys. Acta Gen. . Subj 127:2285–94
     [Google Scholar]
  19. 19. 
    Dilworth MJ, Eady RR, Robson RL, Miller RW 1987. Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo. Nature 327:6118167–68
     [Google Scholar]
  20. 20. 
    Dingler C, Kuhla J, Wassink H, Oelze J 1988. Levels and activities of nitrogenase proteins in Azotobacter vinelandii grown at different dissolved oxygen concentrations. J. Bacteriol. 170:52148–52
     [Google Scholar]
  21. 21. 
    Dixon R, Kahn D. 2004. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2:8621–31
     [Google Scholar]
  22. 22. 
    Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon RC 2012. Distribution of nitrogen fixation and nitrogenase-like gene sequences amongst microbial genomes. BMC Genomics 13:162–73
     [Google Scholar]
  23. 23. 
    Eady RR. 1996. Structure−function relationships of alternative nitrogenases. Chem. Rev. 96:73013–30
     [Google Scholar]
  24. 24. 
    Edgren T, Nordlund S. 2004. The fixABCX genes in Rhodospirillum rubrum encode a putative membrane complex participating in electron transfer to nitrogenase. J. Bacteriol. 186:72052–60
     [Google Scholar]
  25. 25. 
    Einsle O. 2018. Another twist on nitrogenases. Nat. Microbiol. 3:3263–64
     [Google Scholar]
  26. 26. 
    Fixen KR, Chowdhury NP, Martinez-Perez M, Poudel S, Boyd ES, Harwood CS 2018. The path of electron transfer to nitrogenase in a phototrophic alpha-proteobacterium. Environ. Microbiol. 20:72500–8
     [Google Scholar]
  27. 27. 
    Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN et al. 2013. The global nitrogen cycle in the twenty-first century. Philos. Trans. R. Soc. B 368:162120130164
     [Google Scholar]
  28. 28. 
    Gaby JC, Buckley DH. 2011. A global census of nitrogenase diversity. Environ. Microbiol. 13:71790–99
     [Google Scholar]
  29. 29. 
    Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P et al. 2002. The Genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:4532–42
     [Google Scholar]
  30. 30. 
    Gosse JL, Engel BJ, Hui JC-H, Harwood CS, Flickinger MC 2010. Progress toward a biomimetic leaf: 4,000 h of hydrogen production by coating-stabilized nongrowing photosynthetic Rhodopseudomonas palustris. Biotechnol. . Progr 26:4907–18
     [Google Scholar]
  31. 31. 
    Hamilton TL, Ludwig M, Dixon R, Boyd ES, Santos PCD et al. 2011. Transcriptional profiling of nitrogen fixation in Azotobacter vinelandii. J. . Bacteriol 193:174477–86
     [Google Scholar]
  32. 32. 
    Harris DF, Lukoyanov DA, Kallas H, Trncik C, Yang Z-Y et al. 2019. Mo-, V-, and Fe-nitrogenases use a universal eight-electron reductive-elimination mechanism to achieve N2 reduction. Biochemistry 58:303293–301
     [Google Scholar]
  33. 33. 
    Harris DF, Lukoyanov DA, Shaw S, Compton P, Tokmina-Lukaszewska M et al. 2018. Mechanism of N2 reduction catalyzed by Fe-nitrogenase involves reductive elimination of H2. Biochemistry 57:5701–10
     [Google Scholar]
  34. 34. 
    Heiniger EK, Harwood CS. 2015. Posttranslational modification of a vanadium nitrogenase. MicrobiologyOpen 4:4597–603
     [Google Scholar]
  35. 35. 
    Heiniger EK, Oda Y, Samanta SK, Harwood CS 2012. How posttranslational modification of nitrogenase is circumvented in Rhodopseudomonas palustris strains that produce hydrogen gas constitutively. Appl. Environ. Microb. 78:41023–32
     [Google Scholar]
  36. 36. 
    Hill S, Austin S, Eydmann T, Jones T, Dixon R 1996. Azotobacter vinelandii NIFL is a flavoprotein that modulates transcriptional activation of nitrogen-fixation genes via a redox-sensitive switch. PNAS 93:52143–48
     [Google Scholar]
  37. 37. 
    Hodkinson BP, Allen JL, Forrest LL, Goffinet B, Sérusiaux E et al. 2014. Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system. Eur. J. Phycol. 49:111–19
     [Google Scholar]
  38. 38. 
    Hoffman BM, Lukoyanov D, Dean DR, Seefeldt LC 2013. Nitrogenase: a draft mechanism. Accounts Chem. Res. 46:2587–95
     [Google Scholar]
  39. 39. 
    Hoffman BM, Lukoyanov D, Yang Z-Y, Dean DR, Seefeldt LC 2014. Mechanism of nitrogen fixation by nitrogenase: the next stage. Chem. Rev. 114:84041–62
     [Google Scholar]
  40. 40. 
    Hu Y, Lee CC, Ribbe MW 2011. Extending the carbon chain: hydrocarbon formation catalyzed by vanadium/molybdenum nitrogenases. Science 333:6043753–55
     [Google Scholar]
  41. 41. 
    Hu Y, Ribbe MW. 2015. Nitrogenase and homologs. J. Biol. Inorg. Chem. 20:2435–45
     [Google Scholar]
  42. 42. 
    Hu Y, Ribbe MW. 2016. Maturation of nitrogenase cofactor—the role of a class E radical SAM methyltransferase NifB. Curr. Opin. Chem. Biol. 31:188–94
     [Google Scholar]
  43. 43. 
    Huergo LF, Chandra G, Merrick M 2012. PII signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol. Rev. 37:2251–83
     [Google Scholar]
  44. 44. 
    Huergo LF, Dixon R. 2015. The emergence of 2-oxoglutarate as a master regulator metabolite. Microbiol. Mol. Biol. Rev. 79:4419–35
     [Google Scholar]
  45. 45. 
    Huergo LF, Merrick M, Monteiro RA, Chubatsu LS, Steffens MBR et al. 2009. In vitro interactions between the PII proteins and the nitrogenase regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase (DraT) and dinitrogenase reductase-activating glycohydrolase (DraG) in Azospirillum brasilense. J. Biol. . Chem 284:116674–82
     [Google Scholar]
  46. 46. 
    Joerger RD, Bishop PE. 1988. Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii. J. . Bacteriol 170:41475–87
     [Google Scholar]
  47. 47. 
    Khadka N, Dean DR, Smith D, Hoffman BM, Raugei S, Seefeldt LC 2016. CO2 reduction to nitrogenase: pathways to formate, carbon monoxide and methane. Inorg. Chem. 55:8321–30
     [Google Scholar]
  48. 48. 
    Krahn E, Weiss B, Kröckel M, Groppe J, Henkel G et al. 2001. The Fe-only nitrogenase from Rhodobacter capsulatus: identification of the cofactor, an unusual, high-nuclearity iron-sulfur cluster, by Fe K-edge EXAFS and 57Fe Mössbauer spectroscopy. J. Biol. Inorg. Chem. 7:1–237–45
     [Google Scholar]
  49. 49. 
    Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S et al. 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat. . Biotechnol 22:155–61
     [Google Scholar]
  50. 50. 
    Ledbetter RN, Costas AMG, Lubner CE, Mulder DW, Tokmina-Lukaszewska M et al. 2017. The electron bifurcating FixABCX protein complex from Azotobacter vinelandii: generation of low-potential reducing equivalents for nitrogenase catalysis. Biochemistry 56:324177–90
     [Google Scholar]
  51. 51. 
    Lehman LJ, Roberts GP. 1991. Identification of an alternative nitrogenase system in Rhodospirillum rubrum. J. Bacteriol 173:185705–11
     [Google Scholar]
  52. 52. 
    Little R, Reyes‐Ramirez F, Zhang Y, van Heeswijk WC, Dixon R 2000. Signal transduction to the Azotobacter vinelandii NIFL-NIFA regulatory system is influenced directly by interaction with 2-oxoglutarate and the PII regulatory protein. EMBO J 19:226041–50
     [Google Scholar]
  53. 53. 
    Luxem KE, Kraepiel AM, Zhang L, Waldbauer JR, Zhang X 2020. Carbon substrate re-orders relative growth of a bacterium using Mo-, V-, or Fe-nitrogenase for nitrogen fixation. Environ. Microbiol. 22:41397–408
     [Google Scholar]
  54. 54. 
    Lyons EM, Thiel T. 1995. Characterization of nifB, nifS, and nifU genes in the cyanobacterium Anabaena variabilis: NifB is required for the vanadium-dependent nitrogenase. 17761570–75
  55. 55. 
    Madigan M, Cox SS, Stegeman RA 1984. Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. J. Bacteriol. 157:173–78
     [Google Scholar]
  56. 56. 
    Masepohl B, Hallenbeck PC. 2010. Nitrogen and molybdenum control of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus. Adv. Exp. Med. . Biol 675:49–70
     [Google Scholar]
  57. 57. 
    Masepohl B, Krey R, Klipp W 1993. The draTG gene region of Rhodobacter capsulatus is required for post-translational regulation of both the molybdenum and the alternative nitrogenase. J. Gen. Microbiol. 139:112667–75
     [Google Scholar]
  58. 58. 
    McKinlay JB, Harwood CS. 2010. Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. PNAS 107:2611669–75
     [Google Scholar]
  59. 59. 
    McKinlay JB, Harwood CS. 2010. Photobiological production of hydrogen gas as a biofuel. Curr. Opin. Biotechnol. 21:3244–51
     [Google Scholar]
  60. 60. 
    McKinlay JB, Harwood CS. 2011. Calvin cycle flux, pathway constraints, and substrate oxidation state together determine the H2 biofuel yield in photoheterotrophic bacteria. mBio 2:2e00323–10
     [Google Scholar]
  61. 61. 
    McRose DL, Zhang X, Kraepiel AML, Morel FMM 2017. Diversity and activity of alternative nitrogenases in sequenced genomes and coastal environments. Front. Microbiol. 8:205267
     [Google Scholar]
  62. 62. 
    Melis A, Melnicki MR. 2006. Integrated biological hydrogen production. Int. J. Hydrogen Energy 31:111563–73
     [Google Scholar]
  63. 63. 
    Merrick M. 2015. Post-translational modification of PII signal transduction proteins. Front. Microbiol. 5:763
     [Google Scholar]
  64. 64. 
    Mus F, Alleman AB, Pence N, Seefeldt LC, Peters JW 2018. Exploring the alternatives of biological nitrogen fixation. Metallomics 10:4523–38
     [Google Scholar]
  65. 65. 
    Mus F, Colman DR, Peters JW, Boyd ES 2019. Geobiological feedbacks, oxygen, and the evolution of nitrogenase. Free Radic. Biol. Med. 140:250–59
     [Google Scholar]
  66. 66. 
    Nelson J, Hauser D, Gudiño JA, Guadalupe YA, Meeks JC et al. 2019. Complete genomes of symbiotic cyanobacteria clarify the evolution of Vanadium-nitrogenase. Genome Biol. Evol. 11:71959–64
     [Google Scholar]
  67. 67. 
    Newton WE, Dilworth MJ. 2011. Assays of nitrogenase reaction products. Methods Mol. Biol. 766:105–27
     [Google Scholar]
  68. 68. 
    Noda S, Ohkuma M, Usami R, Horikoshi K, Kudo T 1999. Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis. Appl. Environ. Microbiol 65:114935–42
     [Google Scholar]
  69. 69. 
    Nordlund S, Högbom M. 2013. ADP-ribosylation, a mechanism regulating nitrogenase activity. FEBS J 280:153484–90
     [Google Scholar]
  70. 70. 
    Oda Y, Larimer FW, Chain PSG, Malfatti S, Shin MV et al. 2008. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. PNAS 105:4718543–48
     [Google Scholar]
  71. 71. 
    Oda Y, Samanta SK, Rey FE, Wu L, Liu X et al. 2005. Functional genomic analysis of three nitrogenase isozymes in the photosynthetic bacterium Rhodopseudomonas palustris. J. . Bacteriol 187:227784–94
     [Google Scholar]
  72. 72. 
    Oelze J. 2000. Respiratory protection of nitrogenase in Azotobacter species: Is a widely held hypothesis unequivocally supported by experimental evidence. FEMS Microbiol. Rev. 24:4321–33
     [Google Scholar]
  73. 73. 
    Perakis SS, Pett-Ridge JC. 2019. Nitrogen-fixing red alder trees tap rock-derived nutrients. PNAS 116:115009–14
     [Google Scholar]
  74. 74. 
    Phattarasukol SM. 2014. Integrative genomics approach to identify genes important for H2 production by Rhodopseudomonas palustris PhD Thesis, Univ. Wash .
     [Google Scholar]
  75. 75. 
    Pratte BS, Sheridan R, James JA, Thiel T 2013. Regulation of V-nitrogenase genes in Anabaena variabilis by RNA processing and by dual repressors. Mol. Microbiol. 88:2413–24
     [Google Scholar]
  76. 76. 
    Pratte BS, Thiel T. 2005. High-affinity vanadate transport system in the cyanobacterium Anabaena variabilis ATCC 29413. J. Bacteriol. 188:2464–68
     [Google Scholar]
  77. 77. 
    Premakumar R, Lemos E, Bishop P 1984. Evidence for two dinitrogenase reductases under regulatory control by molybdenum in Azotobacter vinelandii. Biochim. Biophys. Acta Gen. . Subj 797:164–70
     [Google Scholar]
  78. 78. 
    Prince RC, Kheshgi HS. 2005. The photobiological production of hydrogen: potential efficiency and effectiveness as a renewable fuel. Crit. Rev. Microbiol. 31:119–31
     [Google Scholar]
  79. 79. 
    Raymond J, Siefert JL, Staples CR, Blankenship RE 2004. The natural history of nitrogen fixation. Mol. Biol. Evol. 21:3541–54
     [Google Scholar]
  80. 80. 
    Rebelein JG, Lee CC, Hu Y, Ribbe MW 2016. The in vivo hydrocarbon formation by vanadium nitrogenase follows a secondary metabolic pathway. Nat. Commun. 7:113641
     [Google Scholar]
  81. 81. 
    Rees DC, Tezcan FA, Haynes CA, Walton MY, Andrade S et al. 2005. Structural basis of biological nitrogen fixation. Philos. Trans. R. Soc. Math. Phys. Eng. Sci. 363:1829971–84
     [Google Scholar]
  82. 82. 
    Remigi P, Zhu J, Young JPW, Masson-Boivin C 2016. Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:163–75
     [Google Scholar]
  83. 83. 
    Rey FE, Heiniger EK, Harwood CS 2007. Redirection of metabolism for biological hydrogen production. Appl. Environ. Microb. 73:51665–71
     [Google Scholar]
  84. 84. 
    Ribbe MW, Hu Y, Hodgson KO, Hedman B 2013. Biosynthesis of nitrogenase metalloclusters. Chem. Rev. 114:84063–80
     [Google Scholar]
  85. 85. 
    Robson RL, Eady RR, Richardson TH, Miller RW, Hawkins M, Postgate JR 1986. The alternative nitrogenase of Azotobacter chroococcum is a vanadium enzyme. Nature 322:6077388–90
     [Google Scholar]
  86. 86. 
    Rousk K, Sorensen PL, Lett S, Michelsen A 2014. Across-habitat comparison of diazotroph activity in the subarctic. Microbial. Ecol. 69:4778–87
     [Google Scholar]
  87. 87. 
    Rubio LM, Ludden PW. 2005. Maturation of nitrogenase: a biochemical puzzle. J. Bacteriol. 187:2405–14
     [Google Scholar]
  88. 88. 
    Schlesier J, Rohde M, Gerhardt S, Einsle O 2015. A conformational switch triggers nitrogenase protection from oxygen damage by Shethna protein II (FeSII). J. Am. Chem. Soc. 138:1239–47
     [Google Scholar]
  89. 89. 
    Seefeldt LC, Peters JW, Beratan DN, Bothner B, Minteer SD et al. 2018. Control of electron transfer in nitrogenase. Curr. Opin. Chem. Biol. 47:54–59
     [Google Scholar]
  90. 90. 
    Seefeldt LC, Yang Z-Y, Duval S, Dean DR 2013. Nitrogenase reduction of carbon-containing compounds. Biochim. Biophys. Acta Bioenerget. 1827: 8–9 1102–11
     [Google Scholar]
  91. 91. 
    Setubal JC, dos Santos P, Goldman BS, Ertesvåg H, Espin G et al. 2009. Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse metabolic processes. J. Bacteriol. 191:144534–45
     [Google Scholar]
  92. 92. 
    Shah VK, Stacey G, Brill WJ 1983. Electron transport to nitrogenase: purification and characterization of pyruvate:flavodoxin oxidoreductase; the nifJ gene product. J. Biol. Chem. 258:1912064–68
     [Google Scholar]
  93. 93. 
    Shimizu T, Teramoto H, Inui M 2019. Engineering the transcriptional activator NifA for the construction of Rhodobacter sphaeroides strains that produce hydrogen gas constitutively. Appl. Microbiol. Biotechnol. 103:23–249739–49
     [Google Scholar]
  94. 94. 
    Sickerman NS, Rettberg LA, Lee CC, Hu Y, Ribbe MW 2017. Cluster assembly in nitrogenase. Essays Biochem 61:2271–79
     [Google Scholar]
  95. 95. 
    Sippel D, Einsle O. 2017. The structure of vanadium nitrogenase reveals an unusual bridging ligand. Nat. Chem. Biol. 13:9956–60
     [Google Scholar]
  96. 96. 
    Sippel D, Rohde M, Netzer J, Trncik C, Gies J et al. 2018. A bound reaction intermediate sheds light on the mechanism of nitrogenase. Science 359:63831484–89
     [Google Scholar]
  97. 97. 
    Stein LY, Klotz MG. 2016. The nitrogen cycle. Curr. Biol. 26:3R94–98
     [Google Scholar]
  98. 98. 
    Thiel T. 1993. Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J. . Bacteriol 175:196276–86
     [Google Scholar]
  99. 99. 
    Thiel T. 1996. Isolation and characterization of the vnfEN genes of the cyanobacterium Anabaena variabilis. J. . Bacteriol 178:154493–99
     [Google Scholar]
  100. 100. 
    van Heeswijk WC, Westerhoff HV, Boogerd FC 2013. Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective. Microbiol. Mol. Biol. Rev. 77:4628–95
     [Google Scholar]
  101. 101. 
    Varghese F, Kabasakal BV, Cotton CAR, Schumacher J, Rutherford AW et al. 2019. A low-potential terminal oxidase associated with the iron-only nitrogenase from the nitrogen-fixing bacterium Azotobacter vinelandii. J. Biol. Chem 294:249367–76
     [Google Scholar]
  102. 102. 
    Wedepohl KH. 1995. The composition of the continental crust. Geochim. Cosmochim. Acta 59:71217–32
     [Google Scholar]
  103. 103. 
    Yang J, Xie X, Wang X, Dixon R, Wang Y-P 2014. Reconstruction and minimal gene requirements for the alternative iron-only nitrogenase in Escherichia coli. . PNAS 111:35E3718–25
     [Google Scholar]
  104. 104. 
    Yang Z-Y, Ledbetter R, Shaw S, Pence N, Tokmina-Lukaszewska M et al. 2016. Evidence that the Pi release event is the rate-limiting step in the nitrogenase catalytic cycle. Biochemistry 55:263625–35
     [Google Scholar]
  105. 105. 
    Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW 1995. Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl. Environ. Microb. 61:72527–32
     [Google Scholar]
  106. 106. 
    Zhang X, McRose DL, Darnajoux R, Bellenger JP, Morel FMM, Kraepiel AML 2016. Alternative nitrogenase activity in the environment and nitrogen cycle implications. Biogeochemistry 127:2–3189–98
     [Google Scholar]
  107. 107. 
    Zhang X, Sigman DM, Morel FMM, Kraepiel AML 2014. Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia. PNAS 111:134782–87
     [Google Scholar]
  108. 108. 
    Zhang Y, Pohlmann EL, Roberts GP 2005. GlnD is essential for NifA activation, NtrB/NtrC-regulated gene expression, and posttranslational regulation of nitrogenase activity in the photosynthetic, nitrogen-fixing bacterium Rhodospirillum rubrum. J. . Bacteriol 187:41254–65
     [Google Scholar]
  109. 109. 
    Zheng Y, Harris DF, Yu Z, Fu Y, Poudel S et al. 2018. A pathway for biological methane production using bacterial iron-only nitrogenase. Nat. Microbiol. 3:3281–86
     [Google Scholar]
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Iron-Only and Vanadium Nitrogenases: Fail-Safe Enzymes or Something More?
Annual Review of Microbiology 74, 247 (2020); https://doi.org/10.1146/annurev-micro-022620-014338
/content/journals/10.1146/annurev-micro-022620-014338
/content/journals/10.1146/annurev-micro-022620-014338
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