Survey on nitrogenase evolution by considering the importance of nitrogenase, its structure, and mechanism of nitrogenase

Authors

  • Wenli SUN National Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing (CN)
  • Mohamad Hesam SHAHRAJABIAN National Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing (CN)

DOI:

https://doi.org/10.15835/nbha52113157

Keywords:

biological nitrogen fixation, nitrogenase, nitrogenase evolution, oxygen, structure of nitrogenase

Abstract

Nitrogenase is a complicated enzyme that actives the ATP-dependent reduction of dinitrogen (N2) to ammonia (NH3). The aim of this manuscript is to review the nitrogenase evolution with considering nitrogenase, structure of nitrogenase, action mechanism of nitrogenase and oxygen sensitive mechanism of nitrogenase. The searches focused on publications from 1980 to February 2023, using PubMed, Google Scholar, Science Direct, and Scopus databases. In the term of evolution, the nitrogen cycle has experienced highly changes; at the beginning of life and suggested the exact anoxic scenario, the comparatively sufficient ammonium was possibly used in an assimilation/mineralization cycle by protocellular organisms. The main nif gene products which are active in nitrogen fixation are nifH, nifD, nifK, nifT, nifY/nafY, nifE, nifN, nifX, nifU, nifS, nifV, nifW, nifZ, nifM, nifF, nifL, nifA, nifB, fdxN, nifQ, and nifJ. The main vnf gene products which are active in nitrogen fixation are vnfA, vnfE, vnfN, vnfX, vnfH, vnfFd, vnfD, vnfG, vnfK, and vnfY. Oxygen can be either detrimental or beneficial for diazotrophs in organisms suitable for an aerobic catabolism, and it supports the production of a substrate for nitrogenase (ATP), but it can also impede the activity and suppress the synthesis of this enzyme. 

References

Akkose S, Gunduz U, Yucel M, Eroglu I (2009). Effects of ammonium ion, acetate and aerobic conditions on hydrogen production and expression levels of nitrogenase genes in Rhodobacter sphaeroides O.U.001. International Journal of Hydrogen Energy 34:8818-8827.https://doi.org/10.1016/j.ijhydene.2009.08.040

Aldasoro J, Larrainzar E, Arrese-Igor C (2019). Application of anti-transpirants temporarily alleviates the inhibition of symbiotic nitrogen fixation in drought-stressed pea plants. Agricultural Water Management 213:193-199. https://doi.org/10.1016/j.agwat.2018.10.014

Allen JF, Thake B, Martin W (2019). Nitrogenase inhibition limited oxygenation of earth’s proterozoic atmosphere. Trends in Plant Science 24(11):1022-1031. https://doi.org/10.1016/j.tplants.2019.07.007

Anbar AD, Knoll AH (2002). Proterozoic ocean chemistry and evolution: A bioionorganic bridge? Science 297:1137-1142. https://doi.org/10.1126/science.1069651

Angove HC, Yoo SJ, Munck E, Burgess BK (1998). An all-ferrous state of the Fe protein of nitrogenase: Interaction with nucleotides and electron transfer to the MoFe protein. Journal of Biological Chemistry 273(41):26330-26337. https://doi.org/10.1074/jbc.273.41.26330

Asad Javed M, Zafar AM, Hassan AA, Zaidi AA, Farooq M, El Badawy A, Lundquist T, Mostafa M, Mohamed MMA, Al-Zuhair S (2022). The role of oxygen regulation and algal growth parameters in hydrogen production via biophotolysis. Journal of Environmental Chemical Engineering 10(1):107003. https://doi.org/10.1016/j.jece.2021.107003

Austin S, Lambert J (1994). Purification and in vitro activity of a truncated form of ANFA. Transcriptional activator protein of alternative nitrogenase from Azotobacter vinelandii. Journal of Biological Chemistry 269(27):18141-18148. https://doi.org/10.1016/s0021-9258(17)32428-6

Banerjee M, Kumar A, Kumar HD (1989). Factors regulating nitrogenase activity and hydrogen evolution in Azolla-anabaena symbiosis. International Journal of Hydrogen Energy 14(12):871-879. https://doi.org/10.1016/0360-3199(89)90074-8

Barbosa HR, Moretti MA, Thuler DS, Augusto EFP (2002). Nitrogenase activity of Beijerinckia derxii preserved under adverse conditions for its growth. Brazilian Journal of Microbiology 33:223-229. https://doi.org/10.1590/s1517-83822002000300007

Barriere F, Pickett CJ, Talarmin J (2001). Extended Huckel calculations on functional and structural models of the FeMo-cofactor of nitrogenase. Polyhedron 20(1-2):27-36. https://doi.org/10.1016/s0277-5387(00)00532-5

Bayer AS, Shepard EM, Peters JW, Broderick JB (2015). Radical S-Adenosyl-L-methionine chemistry in the synthesis of hydrogenase and nitrogenase metal cofactors. Journal of Biological Chemistry 290(7):3987-3994. https://doi.org/10.1074/jbc.r114.578161

Bergmann J, Oksanen E, Ryde U (2021). Critical evaluation of a crystal structure of nitrogenase with bound N2 ligands. Journal of Biological Inorganic Chemistry 26:341-353. https://doi.org/10.1007/s00775-021-01858-8

Bergmann J, Oksanen E, Ryde U (2021). Quantum-refinement studies of the bidentate lignad of v-nitrogenase and the protonation state of CO-inhibited Mo-nitrogenase. Journal of Inorganic Biochemistry 219:111426. https://doi.org/10.1016/j.jinorgbio.2021.111426

Berman J, Gershoni JM, Zamir A (1985). Expression of nitrogen fixation genes in foreign hosts. Assembly of nitrogenase Fe protein in Escherichia coli and in yeast. Journal of Biological Chemistry 260(9):5240-5243. https://doi.org/10.1016/s0021-9258(18)89011-1

Betancourt DA, Loveless TM, Brown JW, Bishop PE (2008). Characterization of diazotrophs containing Mo-independent nitrogenase, isolated from diverse natural environments. Applied and Environmental Microbiology 74:3471-3480. https://doi.org/10.1128/aem.02694-07

Bjornsson R, Neese F, DeBeer S (2017). Revisiting the mssbauer isomer shifts of the FeMoco cluster of nitrogenase and the cofactor charge. Inorganic Chemistry 56 1470-1477. https://doi.org/10.1021/acs.inorgchem.6b02540

Bolin JT, Campobasso N, Muchmore SW, Minor W, Mortenson LE, Morgan TV (1991). The crystal structure of nitrogenase mofe protein from clostridium pasteurianum. Journal of Inorganic Biochemistry 43(2-3):477. https://doi.org/10.1016/0162-0134(91)84457-k

Boyd E, Peters JW (2013). New insights into the evolutionary history of biological nitrogen fixation. Frontiers in Microbiology 4:201. https://doi.org/10.3389/fmicb.2013.00201

Boyd ES, Hamilton TL, Peters JW (2011). An alternative path for the evolution of biological nitrogen fixation. Frontiers in Microbiology 2:1-11. https://doi.org/10.3389/fmicb.2011.00205

Bulen WA, LeComte JR (1966). The nitrogenase system from Azotobacter: two enzyme requirements for N2 reduction, ATP dependent H2 evolution and ATP hydrolysis. Proceedings of the National Academy of Sciences of the USA. 56:979-986. https://doi.org/10.1073/pnas.56.3.979

Burgess BK, Lowe DJ (1996). Mechanism of Molybdenum nitrogenase. Chemical Reviews 96:2983-3012. https://doi.org/10.1021/cr950055x

Chan MK, Kim J, Rees DC (1993). The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Ao resolution structures. Science 260:792-794. https://doi.org/10.1126/science.8484118

Chiu H-J, Peters JW, Lanzilotta WN, Ryle MJ, Seefeldt LC, Howard JB, Rees DC (2001). MgAPT-bound and nucleotide-free structurs of a nitrogenase protein complex between the Leu 127δ-Fe-protein and the MoFe-protein. Biochemistry 40:641-650. https://doi.org/10.1021/bi001645e

Corbett MC, Hu Y, Naderi F, Ribbe MW, Hedman B, Hodgson KO (2004) Comparison of iron-molybdenum cofactor-deficient nitrogenase MoFe proteins by X-ray absorption spectroscopy: Implications for P-cluster biosynthesis. Journal of Biological Chemistry 279(27):28276-28282. https://doi.org/10.1074/jbc.m403156200

CouCouvanis D, Demadis KD, Malinak SM, Mosier PE, Tyson MA, Laughlin LJ (1996). Catalytic and stoichiometric multielectron reduction of hydrazine to ammonia and acetylene to ethylene with clusters that contain the MFe3S4 cores (M=Mo, V). Relevance to the function of nitrogenase. Journal of the American Chemical Society Catalysis A: Chemical 107:123-135. https://doi.org/10.1016/1381-1169(95)00168-9

Curatti L, Brown CS, Ludden PW, Rubio LM, Kustu S (2005). Genes required for rapid expression of nitrogenase activity in Azotobacter vinelandii. Proceedings of the National Academy of Sciences of the USA 102:6291-6296. https://doi.org/10.1073/pnas.0501216102

Curatti L, Hernandez JA, 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. Proceedings of the National Academy of Sciences of the USA 104:17626-17631. https://doi.org/10.1073/pnas.0703050104

Dance I (2013). A molecular pathway for the egress of ammonia produced by nitrogenase. Scientific Reports 3(3237):1-9. https://doi.org/10.1038/srep03237

Danyal K, Shaw S, Page TR, Duval S, Horitani M, Marts AR, Lukoyanov D, Dean DR, Raugei S, Hoffman BM, Seefeldt LC, Antony E (2016). Negative cooperativity in the nitrogenase Fe protein electron delivery cycle. Proceedings of the National Academy of Sciences of the USA E5783-E5791. https://doi.org/10.1073/pnas.1613089113

Davis LC, Kotake S (1980). Regulation of nitrogenase activity in aerobes by MG2+ availability: An hypothesis. Biochemical and Biophysical Research Communications 93(3):934-940. https://doi.org/10.1016/0006-291x(80)91165-1

Dean DR, Bolin JT, Zheng L (1993). Nitrogenase metalloclusters: Structures, organization, and synthesis. Journal of Bacteriology 175:6737-6744. https://doi.org/10.1128/jb.175.21.6737-6744.1993

Del Castillo LD, Hunt S, Layzell DB (1994). The role of oxygen in the regulation of nitrogenase activity in drought-stressed soybean nodules. Plant Physiology 106:949-955. https://doi.org/10.1104/pp.106.3.949

Djekoun A, Planchon C (1991). Water status effect on dinitrogen fixation and photosynthesis in soybean. Agronomy Journal 83:316-322. https://doi.org/10.2134/agronj1991.00021962008300020011x

Dos Santos PC, Mayer SM, Barney BM, Seefeldt LC, Dean DR (2007). Alkyne substrate interaction within the nitrogenase MoFe protein. Journal of Inorganic Biochemistry 101:1642-1648. https://doi.org/10.1016/j.jinorgbio.2007.05.007

Duval S, Danyal K, Shaw S, Lytle AK, Dean DR, Hoffman BM, Antony E, Seefeldt LC (2013). Electron transfer precedes ATP hydrolysis during nitrogenase catalysis. Proceedings of the National Academy of Sciences of the U.S.A 110(41):16414-16419. https://doi.org/10.1073/pnas.1311218110

Eady RR, Postgate JR (1974). Nitrogenase. Nature 249:805-810. https://doi.org/10.1038/249805a0

Eady RR, Prevent DN (1996). Structure-function relationships of alternative nitrogenases. Chemical Reviews 96:3013-3030. https://doi.org/10.1021/cr950057h

Einsle O, Rees DC (2020). Structural enzymology of nitrogenase enzymes. Chemical Reviews 120(12):4969-5004. https://doi.org/10.1021/acs.chemrev.0c00067

Einsle O, Tezcan FA, Andrade SL, Schmid B, Yoshida M, Howard JB, Rees DC (2002). Nitrogenase MoFe-protein at 1.16 A resolution: a central ligand in the FeMo-cofactor. Science 297:1696-1700. https://doi.org/10.1126/science.1073877

Erickson BE, Helz GR (2000). Molybdenum (VI) speciation in sulfidic waters: stability and lability of thiomolybdates. Geochimica et Cosmochimica Acta 64:1149-1158. https://doi.org/10.1016/s0016-7037(99)00423-8

Esfandiary M, Soleymani A, Shahrajabian MH (2012). Evaluation yield and yield components of corn cultivars in different planting methods in semi-arid condition of Iran. Journal of Food, Agriculture and Environment 10(2):664-667.

Esfandiary M, Soleymani A, Shahrajabian MH, Darkhal H (2011). Effect of planting methods on grain yield and leaf orientation at different stages of corn cultivars. Research on Crops 12(2):336-340.

Esteves-Ferreira A, Cavalcanti JHF, Vaz MGMV, Alvarenga LV, Nunes-Nesi A, Araujo WL (2017). Cyanobacterial nitrogenase: phylogenetic diversity, regulation and functional predictions. Gene Molecular Biology 40(1):261-275. https://doi.org/10.1590/1678-4685-gmb-2016-0050

Fani R, Gallo R, Lio P (2000). Molecular evolution of nitrogen fixation: The evolutionary history of the nifD, nifK, nifE, and nifN genes. Journal of Molecular Evolution 51:1-11. https://doi.org/10.1007/s002390010061

Fay AW, Hu Y, Schmid B, Ribbe MW (2007). Molecular insights into nitrogenase FeMoco insertion- The role of His 274 and His 451 of MoFe protein α subunit. Journal of Inorganic Biochemistry 101(11-12):1630-1641. https://doi.org/10.1016/j.jinorgbio.2007.03.013

Fischer HM (1994). Genetic regulation of nitrogen fixation in Rhizobia. Microbiological Reviews 58:352-386. https://doi.org/10.1128/mr.58.3.352-386.1994

Gallon JR (1981). The oxygen sensitivity of nitrogenase: a problem for biochemists and micro-organisms. Trends in Biochemical Sciences 6:19-23. https://doi.org/10.1016/0968-0004(81)90008-6

George SJ, Igarashi RY, Xiao Y, Hernande JA, Demuez M, Zhao D, Yoda Y, Ludden PW, Rubio LM, Cramer SP (2008). Extended X-ray absorption fine structure and nuclear resonance vibrational spectroscopy reveal that NifB-co, a FeMo-co precursor, comprises a 6Fe core with an interstitial light atom. Journal of the American Chemical Society 130:5673-5680. https://doi.org/10.1021/ja0755358

Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC (1992). Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 257(5077):1653-1659. https://doi.org/10.1126/science.1529353

Gerloff DL, Jenny TF, Knecht LJ, Gonnet GH, Benner SA (1993). The nitrogenase MoFe protein. FEBS Letters 318(2):118-124. https://doi.org/10.1016/0014-5793(93)80004-e

Goldberg I, Nadler V, Hochman A (1987). Mechanism of nitrogenase switch-off by oxygen. Journal of Bacteriology 169:874-879. https://doi.org/10.1128/jb.169.2.874-879.1987

Guasch LM, Felipe MRD, Fernandez-Pascual M (2001). Effects of different O2 concentrations on nitrogenase activity, respiration, and O2 diffusion resistance in Lupinus albus L. cv. Multolupa nodules. Journal of Plant Physiology 158(11):1395-1402. https://doi.org/10.1078/0176-1617-00577

Guerrero MG, Vega JM, Losada M (1981). The assimilatory nitrate-reducing system and its regulation. Annual Review of Plant Physiology 32:169-204. https://doi.org/10.1146/annurev.pp.32.060181.001125

Hageman RV, Burris RH (1978). Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Proceedings of the National Academy of Sciences of the USA 75:2699-2702. https://doi.org/10.1073/pnas.75.6.2699

Halbleib CM, Ludden PW (2000). Regulation of biological nitrogen fixation. The Journal of Nutrition 132(12):1081-1084. https://doi.org/10.1093/jn/130.5.1081

Hales BJ, Oliver ME (1991). Investigation of the structure of nitrogenase from magnetic interactions. Journal of Inorganic Biochemistry 43(2-3):478. https://doi.org/10.1016/0162-0134(91)84458-l

Hallenbeck PC (1992). Mutations affecting nitrogenase switch-off in Rhodobacter capsulatus. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology 1118(2):161-168. https://doi.org/10.1016/0167-4838(92)90145-4

Harris D, Lukoyanov S, Shar PD, Compton M, Tokmina-Lukaszewska M, Bothner B, Kelleher NL, Dean DR, Hoffman BM, Seefeldt LC (2017). The mechanism of N2 reduction catalyzed by Fe-nitrogenase involves reductive elimination of H2. Biochemistry 57(5):701-710. https://doi.org/10.1021/acs.biochem.7b01142

Harris DF, Jimenez-Vicente E, Yang Z-Y, Hoffman BM, Dean DR, Seefeldt LC (2020). CO as a substrate and inhibitor of H+ reduction for the Mo-, V-, and Fe-nitrogenase isozymes. Journal of Inorganic Biochemistry 213:111278. https://doi.org/10.1016/j.jinorgbio.2020.111278

Hartmann LS, Barnum SR (2010). Inferring the evolutionary history of Mo-dependent nitrogen fixation from phylogenetic studies of nifK and nifDK. Journal of Molecular Evolution 71:70-85. https://doi.org/10.1007/s00239-010-9365-8

Hernandez JA, Igarashi RY, Soboh B, Curatti L, Dean DR, Ludden PW, Rubio LM (2007). NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Molecular Microbiology 63:177-192. https://doi.org/10.1111/j.1365-2958.2006.05514.x

Hill S (1988). How is nitrogenase regulated by oxygen? FEMS Microbiology Letters 54(2):111-129. https://doi.org/10.1111/j.1574-6968.1988.tb02738.x

Hoffman BM, Dead DR, Seefeldt LC (2009). Climbing nitrogenase: Toward a mechanism of enzymatic nitrogen fixation. Accounts of Chemical Research 42(5):609-619. https://doi.org/10.1021/ar8002128

Hoffman BM, Lukoyanov D, Yang Z-Y, Dean DR, Seefeldt LC (2014). Mechanism of nitrogen fixation by nitrogenase: The next stage. Chemical Reviews 114:4041-4062. https://doi.org/10.1021/cr400641x

Hu Y, Fay AW, Lee CC, Ribbe MW (2007). P-cluster maturation on nitrogenase MoFe protein. Proceedings of the National Academy of Sciences of the USA 104:10424-10429. https://doi.org/10.1073/pnas.0704297104

Hu Y, Lee CC, Ribbe MW (2012). Vanadium nitrogenase: A two-hit wonder? Dalton Transactions 41:1118-1127. https://doi.org/10.1039/c1dt11535a

Hu Y, Ribbe MW (2011). Biosynthesis of nitrogenase FeMoco. Coordination Chemistry Reviews 255(9-10):1218-1224. https://doi.org/10.1016/j.ccr.2010.11.018

Hu Y, Ribbe MW (2013). Nitrogenase assembly. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1827(8-9):1112-1122. https://doi.org/10.1016/j.bbabio.2012.12.001

Hu Y, Ribbe MW (2016). Maturation of nitrogenase cofactor- the role of a class E radical SAM methyltransferase NifB. Current Opinion in Chemical Biology 31:188-194. https://doi.org/10.1016/j.cbpa.2016.02.016

Hu Y, Yoshizawa JM, Fay AW, Lee CC, Wiig JA, Ribbe MW (2009). Catalytic activities of NifEN: implications for nitrogenase evolution and mechanism. Proceedings of the National Academy of Sciences of the USA 106:16962-16966. https://doi.org/10.1073/pnas.0907872106

Huang Q, Tokmina-Lukaszewska M, Johnson LE, Kallas H, Ginovska B, … Raugei S (2021). Mechanical coupling in the nitrogenase complex. PLOS Computational Biology 17(3):e1008719. https://doi.org/10.1371/journal.pcbi.1008719

Igarashi RY, Seefeldt LC (2003). Nitrogen fixation: the mechanism of the mo-dependent nitrogenase. Critical Reviews in Biochemistry and Molecular Biology 38:251-384. https://doi.org/10.1080/10409230391036766

Janas Z, Sobota P (2005). Aryloxo and thiolato vanadium complexes as chemical models of the active site of vanadium nitrogenase. Coordination Chemistry Reviews 249(21-22):2144-2155. https://doi.org/10.1016/j.ccr.2005.04.007

Jasniewski AJ, Sickerman NS, Hu Y, Ribbe MW (2018). The Fe protein: An unsung hero of nitrogenase. Inorganic 6(25):1-14. https://doi.org/10.3390/inorganics6010025

Jiang J, Wang Y, Yu D, Zhu G, Cao Z, Yan G, Li Y (2021). Comparative evaluation of biochar, pelelith, and garbage enzyme on nitrogenase and nitrogen-fixing bacteria during composting of sewage sludge. Bioresource Technology 333:125165. https://doi.org/10.1016/j.biortech.2021.125165

Johnson JL, Nyborg AC, Wilson PE, Tolley AM, Nordmeyer FR, Watt GD (2000). Analysis of steady state Fe and MoFe protein interactions during nitrogenase catalysis. Biochimica et Biophysica Acta 1543:24-35. https://doi.org/10.1016/s0167-4838(00)00195-3

Joseph C, Shupp JP, Cobb CR, Rose MJ (2020). Construction of synthetic models for nitrogenase-relevant NifB biogenesis intermediates and iron-carbide-sulfide clusters. Catalysts 10(1317):1-22. https://doi.org/10.3390/catal10111317

Kang W, Lee CC, Jasniewski AJ, Ribbe MW, Hu Y (2020). Structural evidence for a dynamic metallocofactor during N2 reduction by Mo-nitrogenase. Science 368(6497):1381-1385. https://doi.org/10.1126/science.aaz6748

Kangatharalingam M, Priscu JC, Paerl HW (1992). Heterocyst envelope thickness, heterocyst frequency and nitrogenase activity in Anabaena flos-aquae: influence of exogenous oxygen tension. The Journal of General Microbiology 138:2673-2678. https://doi.org/10.1099/00221287-138-12-2673

Karthik C, Elangovan N, Kumar TS, Govindharaju S, Barathi S, Oves M, Arulselvi PI (2017). Characterization of multifarious plant growth promoting traits of rhizobacteria strain AR6 under chromium (VI) stress. Microbiological Research 204:65-71. https://doi.org/10.1016/j.micres.2017.07.008

Keable SM, Zadvornyy OA, Johnson LE, Ginovska B, Rasmussen AJ, Danyal K, Eilers BJ, Prussia GA, LeVan AX, Raugei S, Seefeldt LC, Peters JW (2018). Structural characterization of the P1+ intermediate state of the P-cluster of nitrogenase. Journal of Biological Chemistry 293(25):9629-9635. https://doi.org/10.1074/jbc.ra118.002435

Khademian M, Imlay JA (2021). How microbes evolved to tolerate oxygen. Trends in Microbiology 29(5):428-440. https://doi.org/10.1016/j.tim.2020.10.001

Khoshkharam M, Rezaei A, Soleymani A, Shahrajabian MH (2010). Effects of tillage and residue management on yield components and yield of maize in second cropping after barley. Research on Crops 11(3):659-666.

Khoshkharam M, Shahrajabian MH, Esfandiary M (2021). The effects of methanol and amino acid glycine betaine on qualitative characteristics and yield of sugar beet (Beta vulgaris L.). Notulae Scientia Biologicae 13(2):1-13.

Kim J, Rees DC (1992). Crystallographic structure and functional implications of the nitrogenase molybdenum-iron protein from Azotobacter vinelandii. Nature (London) 360:553-560. https://doi.org/10.1038/360553a0

Kim S, Burgess BL (1996). Evidence for the direct interaction of the nifW gene product with the MoFe protein. Journal of Biological Chemistry 271:9764-9770. https://doi.org/10.1074/jbc.271.16.9764

Kowalska J, DeBeer S (2015). The role of X-ray spectroscopy in understanding the geometric and electronic structure of nitrogenase. Biochimica et Biophysica Acta 183:1406-1415. https://doi.org/10.1016/j.bbamcr.2014.11.027

Kumar A, Kumar HD (1988). Nitrogen-fixation by blue-green algae. In: Sen SP (Ed). Proceedings of the Plant Physiology Research, Society for Plant Physiology and Biochemistry, 1st International Congress of Plant Physiology, New Delhi, India, pp 85-103.

Kumar A, Sinha RP, Hader D-P (1996). Effect of UV-B on enzymes of nitrogen metabolism in the Cyanobacterium Nostoc calcicola. Journal of Plant Physiology 148:86-91. https://doi.org/10.1016/s0176-1617(96)80298-7

Kumar D, Pandey AB, Kumar HD (1990). Effect of some physiological factors on the nitrogenase and hydrogenase of the Azolla-Anabaena Azollae association. International Journal of Hydrogen Energy 15(5):313-317. https://doi.org/10.1016/0360-3199(90)90178-2

Lancaster K, Roemelt M, Ettenhuber P, Hu Y, Ribbe MW, Neese F, Bergmann U, DeBeer S (2011). X-ray emission spectroscopy evidences a central carbon in the nitrogenase iron-molybdenum cofactor. Science 2011:974-977. https://doi.org/10.1126/science.1206445

Lanzilotta WN, Fisher K, Seefeldt LC (1997). Evidence for electron transfer-dependent formation of a nitrogenase iron protein-molybdenum-iron protin tight complex: The role of aspartate 39. Journal of Biological Chemistry 272(7):4157-4165. https://doi.org/10.1074/jbc.272.7.4157

Lery LMS, Bitar M, Costa MGS, Rossle SCS, Bisch PM (2010). Unraveling the molecular mechanisms of nitrogenase conformational protection against oxygen in diazotrophic bacteria. BMC Genomics 11(5):1-11. https://doi.org/10.1186/1471-2164-11-s5-s7

Li Y, Ma L, Fu Y, Zhang C, Shi Y, Xu Y, Li J (2022). Sulfurization enhancement of FeMoO4 for electrochemical ammonia synthesis with high faradaic efficiency in neutral media. Journal of Electroanalytical Chemistry 905:115981. https://doi.org/10.1016/j.jelechem.2021.115981

Liu D, Liberton M, Yu J, Pakrasi HB, Bhattacharyya-Pakrasi M (2018). Engineering nitrogen fixation activity in an oxygenic phototroph. mBio 9:e01029-18. https://doi.org/10.1128/mBio.01029-18

Liu S, Liu Y, Zhang J (2021). Proteomic mechanisms for the regulation of growth, photosynthetic activity and nitrogen fixation in Nostoc sp. PCC 7120 exposed to three antibiotic contaminants. Ecotoxicology and Environmental Safety 225:112753. https://doi.org/10.1016/j.ecoenv.2021.112753

Liu Y, Ghosh D, Hallenbeck PC (2015). Biological reformation of ethanol to hydrogen by Rhodopseudomonas palustris CGA009. Bioresource Technology 176:189-195. https://doi.org/10.1016/j.biortech.2014.11.047

Lorite MJ, Estrella MJ, Escaray FJ, Sannazzaro A, Castro, Videira E, Monza IM, Sanjuan J, Leon-Barrios M (2018). The Rhizobia-Lotus symbioses: deeply specific and widely diverse. Frontiers in Microbiology 9:2055. https://doi.org/10.3389/fmicb.2018.02055

Lorite MJ, Videirae Castro I, Munoz S, Sanjuan J (2012). Phylogenetic relationship of Lotus uliginosus symbionts with bradyrhizobia nodulating genistoid legumes. FEMS Microbiology Ecology 79:454-464. https://doi.org/10.1111/j.1574-6941.2011.01230.x

Ma Y, Prasad MN, Rajkumar M, Freitas H (2011). Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances 29(2):248-258. https://doi.org/10.1016/j.biotechadv.2010.12.001

Maeda I, Daba M, Hirose N, Nagao H, Idehara K, Miura Y, Yagi K, Mizoguchi T (1999). Repression of nitrogenase by ethanol in nitrogen-deprived cultures of Rhodovulum sulfidophilum. FEMS Microbiology Letters 171(2):121-126. https://doi.org/10.1111/j.1574-6968.1999.tb13421.x

Marchal K, Vanderleyden J (2000). The “oxygen paradox” of dinitrogen-fixing bacteria. Biology and Fertility of Soils 30:363-373. https://doi.org/10.1007/s003740050017

Mayer SM, Gormal CA, Smith BE, Lawson DM (2002). Crystallographic analysis of the MoFe protein of nitrogenase from a nifV mutant of Klebsiella pneumoniae identifies citrate as a ligand to the molybdenum of iron molybdenum cofactor (FeMoco). Journal of Biological Chemistry 277:35263-35266. https://doi.org/10.1074/jbc.m205888200

McGlynn SE, Boyd ES, Peters JW, Orphan VJ (2012). Classifying the metal dependence of uncharacterized nitrogenases. Frontiers in Microbiology 3:1-8. https://doi.org/10.3389/fmicb.2012.00419

Medina MS, Bretzing KO, Aviles RA, Chong KM, Espinoza A, Garcia CNG, Katz BB, Kharwa RN, Hernandez A, Lee JL, Lee TM, LoVerde C, Strul MW, Wong EY, Owens CP (2021). CowN sustains nitrogenase turnover in the presence of the inhibitor carbon monoxide. Journal of Biological Chemistry 296:100501. https://doi.org/10.1016/j.jbc.2021.100501

Meng S-L, Li X-B, Tung C-H, Wu L-Z (2021). Nitrogenase inspired artificial photosynthetic nitrogen fixation. Chem 7(6):1431-1450. https://doi.org/10.1016/j.chempr.2020.11.002

Miller AF, Orme-Johnson WH (1992). The dependence on iron availability of allocation of iron to nitrogenase components in Klebsiella pneumoniae and Escherichia coli. Journal of Biological Chemistry 267(13):9398-9408. https://doi.org/10.1016/s0021-9258(19)50437-9

Misra HS (1999). Oxygen implication in the diazotrophic growth of Plectonema boryanum in dark-light cycles. Plant Science 143(2):135-142. https://doi.org/10.1016/s0168-9452(99)00047-3

Murry MA, Horne AJ, Benemann JR (1984). Physiological studies of oxygen protection mechanisms in the heterocysts of Anabaena cylindrical. Environmental Microbiology 47:449-454. https://doi.org/10.1128/aem.47.3.449-454.1984

Mus F, Alleman AB, Pence N, Seefeldt LC, Peters JW (2018). Exploring the alternatives of biological nitrogen fixation. Metallomics 10:523-538. https://doi.org/10.1039/c8mt00038g

Mus F, Colman DR, Peters JW, Boyd ES (2019). Geobiological feedbacks, oxygen, and the evolution of nitrogenase. Free Radical Biology & Medicine 140:250-259. https://doi.org/10.1016/j.freeradbiomed.2019.01.050

Navarro-Gonzalez R, McKay CP, Mvondo DN (2001). A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412:61-64. https://doi.org/10.1038/35083537

Neubauer U, Nowack B, Furrer G, Schulin R (2000). Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environmental Science & Technology 34(13). https://doi.org/10.1021/es990495w

Nomata J, Kitashima M, Inoue K, Fujita Y (2006). Nitrogenase Fe protein-like Fe-S cluster is conserved in L-protein (BchL) of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. FEBS Letters 580(26):6151-6154. https://doi.org/10.1016/j.febslet.2006.10.014

Nordlund S, Hogbom M (2013). ADP-ribosylation, a mechanism regulating nitrogenase activity. The FEBS Journal 280:3484-3490. https://doi.org/10.1111/febs.12279

Oelze J (2000). Respiratory protection of nitrogenase in Azotobacter species: is a widely held hyptothesis unequivocally supported by experimental evidence? FEMS Microbiology Reviews 24(4):321-333. https://doi.org/10.1111/j.1574-6976.2000.tb00545.x

Ogbaji PO, Li J, Xue X, Shahrajabian MH, Eneji AE (2018). Mineralogical and textural characteristics of soils of Hancheng and Shannxi province, China. Communications in Soil Science and Plant Analysis 49(2):1-5. https://doi.org/10.1080/00103624.2017.1421217

Ogbaji PO, Shahrajabian MH, Xue X (2013). Changes in germination and primarily growth of three cultivars of tomato under diatomite and soil materials in auto-irrigation system. International Journal of Biological Sciences 5(3):80-84. https://doi.org/10.5539/ijb.v5n3p80

Oh CJ, Kim HB, Kim J, Kim WJ, Lee H, An CS (2012). Organization of nif gene cluster in Frankia sp. EuIK1 strain, a symbiont of Elaeagnus umbellata. Archives of Microbiology 194:29-34. https://doi.org/10.1007/s00203-011-0732-7

Orme-Johnson WH (1985). Molecular basis of biological nitrogen fixation. Annual Review of Biophysics Chemistry 14:419-459. https://doi.org/10.1146/annurev.bb.14.060185.002223

Pence N, Lewis N, Alleman AB, Seefeldt LC, Peters JW (2021). Revealing a role for the G subunit in mediating interactions between the nitrogenase component proteins. Journal of Inorganic Biochemistry 214:111273. https://doi.org/10.1016/j.jinorgbio.2020.111273

Peters JW, Fisher K, Dean DR (1995). Nitrogenase structure and function: a biochemical-genetic perspective. Annual Review of Microbiology 49:335-366. https://doi.org/10.1146/annurev.mi.49.100195.002003

Peters JW, Szilagyi RK (2006). Exploring new frontiers of nitrogenase structure and mechanism. Current Opinion in Chemical Biology 10(2):101-108. https://doi.org/10.1016/j.cbpa.2006.02.019

Pierik A, Wassink H, Haaker H, Hagen WR (1993). Redox properties and EPR spectroscopy of the P-clusters of Azotobacter vinelandii MoFe protein. European Journal of Biochemistry 1993:51-61. https://doi.org/10.1111/j.1432-1033.1993.tb17632.x

Plies-Balzer E, Kong T, Schubert S, Mengel K (1995). Effect of water stress on plant growth, nitrogenase activity and nitrogen economy of four different cultivars of Vicia faba L. European Journal of Agronomy 4(2):167-173. https://doi.org/10.1016/s1161-0301(14)80043-9

Raymond J, Siefert JL, Staples CR, Blankenship RE (2004). The natural history of nitrogen fixation. Molecular Biology and Evolution 21:41-554. https://doi.org/10.1093/molbev/msh047

Rees DC, Howard JB (2000). Nitrogenase: standing at the crossroads. Current Opinion in Chemical Biology 4(5):559-566. https://doi.org/10.1016/s1367-5931(00)00132-0

Riaziat A, Soleymani A, Shahrajabian MH (2012). Changes in seed yield and biological yield of six wheat cultivars on the basis of different sowing dates. Journal of Food, Agriculture and Environment 10(1):467-469.

Richards RL (1996). Reactions of small molecules at transition metal sites: studies relevant to nitrogenase, an organometallic enzyme. Coordination Chemistry Reviews 154:83-97. https://doi.org/10.1016/0010-8545(96)01186-1

Rubio LM, Ludden PW (2005). Maturation of nitrogenase: a biochemical puzzle. Journal of Bacteriology 187(2):405-414. https://doi.org/10.1128/jb.187.2.405-414.2005

Rubio LM, Ludden PW (2008). Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annual Review Microbiology 62:93-111. https://doi.org/10.1146/annurev.micro.62.081307.162737

Rutten PJ, Poole PS (2019). Oxygen regulatory mechanisms of nitrogen fixation in rhizobia. Advances in Microbial Physiology 75:325-389. https://doi.org/10.1016/bs.ampbs.2019.08.001

Sarma R, Barney BM, Keable S, Dean DR, Seefeldt LC, Peters JW (2010). Insights into substrate binding at FeMo-cofactor in nitrogenase from the structure of an α-70Ile MoFe protein variant. Journal of Inorganic Biochemistry 104(4):385-389. https://doi.org/10.2210/pdb3k1a/pdb

Seefeldt LC, Hoffman BM, Dean DR (2009). Mechanism of Mo-dependent nitrogenase. Annual Review Biochemistry 78(701):1-28. https://doi.org/10.1146/annurev.biochem.78.070907.103812

Seefeldt LC, Hoffman BM, Dean DR (2012). Electron transfer in nitrogenase catalysis. Current Opinion in Chemical Biology 16:19-25. https://doi.org/10.1016/j.cbpa.2012.02.012

Seefeldt LC, Yang Z-Y, Duval S, Dean DR (2013). Nitrogenase reduction of carbon-containing compounds. Biochimica et Biophysica Acta 1827:1102-1111. https://doi.org/10.1016/j.bbabio.2013.04.003

Sellmann D, Fursattel A, Sutter J (2000). The nitrogenase catalyzed N2 dependent HD formation: a model reaction and its significance for the FeMoco function. Coordination Chemistry Reviews 200-202:545-561. https://doi.org/10.1016/s0010-8545(99)00240-4

Shah VK, Allen JR, Spangler NJ, Ludden PW (1994). In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Purification and characterization of NifB cofactor, the product of NifB protein. Journal of Biological Chemistry 269:1154-1158. https://doi.org/10.1016/s0021-9258(17)42235-6

Shah VK, Brill WJ (1973). Nitrogenase. IV. Simple method of purification to homogeneity of nitrogenase components from Azotobacter vinelandii. Biochimica et Biophysica Acta 305:445-454. https://doi.org/10.1016/0005-2728(73)90190-4

Shahrajabian MH, Chaski C, Polyzos N, Petropoulos SA (2021a). Biostimulants application: A low input cropping management tool for sustainable farming vegetables. Biomolecules 11(5):698. https://doi.org/10.3390/biom11050698

Shahrajabian MH, Chaski C, Polyzos N, Tzortzakis N, Petropoulos SA (2021b). Sustainable agriculture systems in vegetable production using chitin and chitosan as plant biostimulants. Biomolecules 11(6):819. https://doi.org/10.3390/biom11060819

Shahrajabian MH, Khoshkharam M, Sun W, Cheng Q (2020a). The influence of increased plant densities and nitrogen fertilizer levels on forage yield, seed yield and qualitative characteristics of forage sorghum (Sorghum bicolor L. Moench). Thai Journal of Agricultural Science 53(4):201-217.

Shahrajabian MH, Soleymani A, Naranjani L (2011). Grain yield and forage characteristics of forage sorghum under different plant densities and nitrogen levels in second cropping after barley in Isfahan, Iran. Research on Crops 12(1):68-78.

Shahrajabian MH, Sun W, Cheng Q (2019a). Sustainable agriculture and soybean, a legume in traditional Chinese medicine with great biological nitrogen fixation. Journal of Biological & Environmental Sciences 13(38):71-78.

Shahrajabian MH, Sun W, Cheng Q (2019b). Measures to achieve a stable farming system in sustainable agriculture- a short review. Annales Universitatis Paedagogicae Cracoviensis Studia Naturae 4(4):172-181. https://doi.org/10.24917/25438832.4.11

Shahrajabian MH, Sun W, Cheng Q (2022). Foliar application of nutrients on medicinal and aromatic plants, the sustainable approaches for higher and better production. Beni-Suef University Journal of Basic & Applied Sciences 11(26):1-10. https://doi.org/10.1186/s43088-022-00210-6

Shahri MH, Soleymani A, Shahrajabian MH, Yazdpour H (2012). Effect of plant densities and sulphur fertilizer on seed and oil yields of canola. Research on Crops 12(2):383-387.

Shayanfar M, Soleymani A, Shahrajabian MH (2011). Effect of plant densities on solar radiation absorption and depreciation, leaf area index and crop growth rate of different cultivars of sunflower. Research On Crops 12(3):728-730.

Shepard EM, Boyd ES, Broderick JB, Peters JW (2011). Biosynthesis of complex iron-sulfur enzymes. Current Opinion Chemical Biology 15:319-327. https://doi.org/10.1016/j.cbpa.2011.02.012

Shilov AE (1987). Catalytic reduction of dinitrogen in protic media: chemical models of nitrogenase. Journal of Molecular Catalysis 41(1-2):221-234. https://doi.org/10.1016/0304-5102(87)80030-5

Sickerman NS, Tanifuji K, Hu Y, Ribbe MW (2017). Synthetic analogues of nitrogenase metallocofactors: challenges and developments. Chemistry 23:12425-12432. https://doi.org/10.1002/chem.201702496

Siegbahn PEM (2019). The mechanism for nitrogenase including all steps. Physical Chemistry Chemical Physics 21:15747-15759. https://doi.org/10.1039/c9cp02073j

Simpson FB, Burris RH (1984). A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095-1097. https://doi.org/10.1126/science.6585956

Sippel D, Einsle O (2017). The structure of vanadium nitrogenase reveals an unusual bridging ligand. Nature Chemical Biology 13:956-960. https://doi.org/10.1038/nchembio.2428

Skizim NJ, Ananyev GM, Krishnan A, Dismukes GC (2012). Metabolic pathways for photobiologial hydrogen production by nitrogenase- and hydrogenase-containing unicellular cyanobacteria Cyanothece. Journal of Biological Chemistry 287(4):2777-2786. https://doi.org/10.1074/jbc.m111.302125

Smith BE (1977). The structure and function of nitrogenase: A review of the evidence for the role of molybdenum. Journal of the Less Common Metals 54(2):465-475. https://doi.org/10.1016/0022-5088(77)90069-8

Smith RL, Tabita FR, Baalen CV (1988) Hydrogen uptake in Anabaena sp. strain CA does not protect nitrogenase from inactivation by hyperbaric oxygen. FEMS Microbiology Letters 52(3):183-187.https://doi.org/10.1111/j.1574-6968.1988.tb02592.x

Soboh B, Boyd ES, Zhao D, Peters JW, Rubio LM (2010). Substrate specificity and evolutionary implications of a NifDK enzyme carrying NifB-co at its active site. FEBS Letters 584:1487-1492. https://doi.org/10.1016/j.febslet.2010.02.064

Soleymani A, Hoodaji M, Shahrajabian MH, Karimi A (2011b). The influence of manganese sulfate on yield and yield components of three wheat cultivars in Abadeh region. Journal of Food, Agriculture and Environment 9(3-4):247-248.

Soleymani A, Shahrajabian MH, Khoshkharam M (2016). The impact of barley residue management and tillage on forage maize. Romanian Agricultural Research 33:161-167.

Soleymani A, Shahrajabian MH, Naranjani L (2011a). The effect of plant density and nitrogen fertilization on yield, yield components and grain protein of grain sorghum. Journal of Food, Agriculture and Environment 9(3):244-246.

Soleymani A, Shahrajabian MH, Naranjani L (2013). Effect of planting dates and different levels of nitrogen on seed yield and yield components of nuts sunflower (Helianthus annuus L.). African Journal of Agricultural Research 8(46):5802-5805.

Som SM, Buick R, Hagadorn JW, Blake TS, Perreault JN, Harnmeijer JP, Catling DC (2016). Earth’s air pressure 2.7 billion years ago constrained to less than half of modern levels. Nature Geoscience 9:448-452. https://doi.org/10.1038/ngeo2713

Soto-Urzua L, Baca BE (2001). Protection mechanisms of nitrogenase to inactivation by oxygen. Revista Latinoamericana de Microbiologia 43(1):37-49. https://doi.org/10.1139/m96-043

Stal LJ (2017). The effect of oxygen concentration and temperature on nitrogenase activity in the heterocystous activity in the heterocystous cyanobacterium Fischerella sp. Scientific Reports 7(5402):1-10. https://doi.org/10.1038/s41598-017-05715-0

Stams AJM (1994). Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie van Leeuwenhoek 66:271-294. https://doi.org/10.1007/bf00871644

Streeter JG (1995). A new model for the rapid effects of non-invasive treatment on nitrogenase and respiratory activity in legume nodules. Journal of Theoretical Biology 174:441-452. https://doi.org/10.1006/jtbi.1995.0110

Sujkowska-Rybkowska M, Banasiewicz J, Rekosz-Burlaga H, Stepkowski T (2020). Anthyllis vulneraria and Lotus corniculatus on calamine heaps from nodules with Bradyrhizobium liaoningense-related strains harboring novel in Europe symbiotic nifD haplotypes. Applied Soil Ecology 151:103539. https://doi.org/10.1016/j.apsoil.2020.103539

Sun W, Shahrajabian MH (2023). The application of arbuscular mycorrhizal fungi as microbial biostimulant, sustainable approaches in modern agriculture. Plants 12(17):3101. https://doi.org/10.3390/plants12173101

Sun W, Shahrajabian MH, Cheng Q (2021). Nitrogen fixation and diazotrophs-A review. Romanian Biotechnological Letters 26(4):2834-2845. https://doi.org/10.25083/rbl/26.4/2834-2845

Sun W, Shahrajabian MH, Petropoulos SA, Shahrajabian N (2023). Developing sustainable agriculture systems in medicinal and aromatic plant production by using chitosan and chitin-based biostimulants. Plants 12(13):2469. https://doi.org/10.3390/plants12132469

Tal S, Chun TW, Gavini N, Burgess BK (1991). The delta-nifB (or delta-nifE) FeMo cofactor-deficient MoFe protein is different from the delta-nifH protein. Journal of Biological Chemistry 266: 10654-10657. https://doi.org/10.1016/s0021-9258(18)99273-2

Tejera NA, Campos R, Sanjuan J, Lluch C (2004). Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. Journal of Plant Physiology 161(3):329-338. https://doi.org/10.1078/0176-1617-01050

Thiel T, Pratte BS (2014). Regulation of three nitrogenase gene clusters in the cyanobacterium Anabaena variabilis ATCC29413. Life 4:944-967. https://doi.org/10.3390/life4040944

Tian B, Gao W, Ning X, Wu Y, Lu G (2019). Enhancing water splitting activity by protecting hydrogen evolution activity site from poisoning of oxygen species. Applied Catalysis B: Environmental 249:138-146. https://doi.org/10.1016/j.apcatb.2019.02.051

Tibbles BJ, Lucas MI, Coyne VE, Newton ST (1994). Nitrogenase activity in marine sediments from a temperate saltmarsh lagoon: modulation by complex polysaccharides, ammonium and oxygen. Journal of Experimental Marine Biology and Ecology 184(1):1-20. https://doi.org/10.1016/0022-0981(94)90163-5

Trncik C, Muller T, Franke P, Einsle O (2022). Structural analysis of the reductase component AnfH of iron-only nitrogenase from Azotobacter vinelandii. Journal of Inorganic Biochemistry 227:111690. https://doi.org/10.1016/j.jinorgbio.2021.111690

Varghese F, Kabasakal BV, Cotton CAR, Schumacher J, Rutherford AW, Fantuzzi A, Murray JW (2019). A low-potential terminal oxidase associated with the iron-only nitrogenase from the nitrogen-fixing bacterium Azotobacter vinelandii. Journal of Biological Chemistry 294(24):9367-9376. https://doi.org/10.1074/jbc.ra118.007285

Vinoth M, Sivasankari S, Ahamed AKK, Al-Arjani A-BF, Abd-Allah EF, Baskar K (2020). Biological soil crust (BSC) is an effective biofertilizer on Vigna mungo (L.). Saudi Journal of Biological Sciences 27:2325-2332. https://doi.org/10.1016/j.sjbs.2020.04.022

Wang C-H, DeBeer S (2021). Structure, reactivity, and spectroscopy of nitrogenase-related synthetic and biological clusters. Chemical Society Reviews 50:8743-8876. https://doi.org/10.1039/d1cs00381j

Wang D (2012). Redox chemistry of molybdenum in natural waters and its involvement in biological evolution. Frontiers in Microbiology 3:1-7. https://doi.org/10.3389/fmicb.2012.00427

Wang D, Zhang Y, Welc, E, Li J, Roberts GP (2010). Elimination of Rubisco alters the regulation of nitrogenase activity and increases hydrogen production in Rhodospirillum rubrum. International Journal of Hydrogen Energy 35(14):7377-85. https://doi.org/10.1016/j.ijhydene.2010.04.183

Wang L, Chen, M, Wei L, Gao F, Lv Z, Wang Q, Ma W (2010). Treatment with moderate concentrations of NaHSO3 enhances photobiological H2 production in the cyanobacterium Anabaena sp. strain PCC 7120. International Journal of Hydrogen Energy 35:12777-12783. https://doi.org/10.1016/j.ijhydene.2010.08.115

Wang L, Zhang L, Liu Z, Zhao D, Liu X, Zhang B, Xie J, Hong Y, Li P, Chen S, Dixon R, Li J (2013). A minimal nitrogen fixation gene cluster from Paenibacillus sp. WLY78 enables expression of active nitrogenase in Escherichia coli. PLOS Genetics 9:1-11. https://doi.org/10.1371/annotation/1e9bcb70-265a-4383-abf4-3466d144d56e

Wang X, Yang H, Zhang Y, Guo L (2014). Remarkable enhancement on hydrogen production performance of Rhodobacter sphaeroides by disrupting spbA and hupSL genes. International Journal of Hydrogen Energy 39(27):14633-41. https://doi.org/10.1016/j.ijhydene.2014.07.061

Webb J, Sheehy JE (1991). Legume nodule morphology with regard to oxygen diffusion and nitrogen fixation. Annals of Botany 67:85-92. https://doi.org/10.1093/oxfordjournals.aob.a088103

Wilson PE, Nyborg AC, Watt GD (2001). Duplication and extension of the Thorneley and Lowe kinetic model for Klebsiella pneumoniae nitrogenase catalysis using a MATHEMATICA software platform. Biophysical Chemistry 91(3):281-304. https://doi.org/10.1016/s0301-4622(01)00182-x

Xie Z, Liu Y, Hu C, Chen L, Li D (2007). Relationships between the biomass of algal crusts in fields and their compressive strength. Soil Biology and Biochemistry 39(2):567-572. https://doi.org/10.1016/j.soilbio.2006.09.004

Yamamoto H, Kato M, Yamanashi K, Fujita Y (2014). Reconstitution of a sequential reaction of two nitrogenase-like enzymes in the bacteriochlorophyll biosynthetic pathway of Rhodobacter capsulatus. Biochemical and Biophysical Research Communications 448(2):200-205. https://doi.org/10.1016/j.bbrc.2014.04.087

Yang H, Wang X, Zhang L, Guo L (2012). Enhanced hydrogen production performance of Rubrivivax gelatiosus M002 using mixed carbon sources. International Journal of Hydrogen Energy 37(18):13296-303. https://doi.org/10.1016/j.ijhydene.2012.06.101

Yang H, Zhang J, Wang X, Feng J, Yan W, Guo L (2015). Coexpression of Mo- and Fe-nitrogenase in Rhodobacter capsulatus enhanced its photosynthetic hydrogen production. International Journal of Hydrogen Energy 40:927-934. https://doi.org/10.1016/j.ijhydene.2014.11.087

Yang J (2019). Progress in synthesizing analogues of nirogenase metalloclusters for catalytic reduction of nitrogen to ammonia. Catalysts 9(939):1-19. https://doi.org/10.3390/catal9110939

Yazdpour H, Shahri MM, Soleymani A, Shahrajabian MH (2012). Effects of harvesting time and harvesting height on grain yield and agronomical characters in rice ratoon (Oryza sativa L.). Journal of Food, Agriculture and Environment 10(1):438-440.

Yong Y, Hu Y-G, Shahrajabian MH, Ren C-Z, Guo L-C, Wang C-L, Zing Z-H (2018). Changes in dry matter, protein percentage and organic matter of soybean-oat and groundnut-oat intercropping in different growth stages in Jilin province, China. Acta Agriculturae Slovenica 111(1): 3-39. https://doi.org/10.14720/aas.2018.111.1.04

Yun AC, Szalay AA (1984). Structural genes of dinitrogenase and dinitrogenase reductase are transcribed from two separate promoters in the broad host range cowpea Rhizobium strain IRc78. Proceedings of the National Academy of Sciences of the USA 81:7358-7362. https://doi.org/10.1073/pnas.81.23.7358

Zanello P (2019). Structure and electrochemistry of proteins harboring iron-sulfur clusters of different nuclearities. Part V. Nitrogenases. Coordination Chemistry Reviews 398:113004. https://doi.org/10.1016/j.ccr.2019.07.001

Zhang X, Sigman DM, Morel, Kraepiel AML (2014). Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia. Proceedings of the National Academy of Sciences of the USA 111:4782-4787. https://doi.org/10.1073/pnas.1402976111

Zheng K, White RH, Dean DR (1997). Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. Journal of Bacteriology 179:5963-5966. https://doi.org/10.1128/jb.179.18.5963-5966.1997

Downloads

Published

2024-02-12

How to Cite

SUN, W., & SHAHRAJABIAN, M. H. (2024). Survey on nitrogenase evolution by considering the importance of nitrogenase, its structure, and mechanism of nitrogenase. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(1), 13157. https://doi.org/10.15835/nbha52113157

Issue

Vol. 52 No. 1 (2024)

Section

Review Articles
CITATION
DOI: 10.15835/nbha52113157

License

Copyright (c) 2024 Wenli SUN, Mohamad Hesam SHAHRAJABIAN

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

License:

© Articles by the authors; licensee UASVM and SHST, Cluj-Napoca, Romania. Papers published in the journal Notulae Botanicae Horti Agrobotanici Cluj-Napoca are open access distributed under the terms and conditions of the Creative Commons Attribution License (http://creativecommons.org/licenses).

Open Access Journal:

The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.

Crossref
Scopus
Google Scholar
Europe PMC