Divergent Members of the Nitrogenase Superfamily: Tetrapyrrole Biosynthesis and Beyond
Abstract
The nitrogenase superfamily constitutes a large and diverse ensemble of two–component metalloenzymes. These systems couple the hydrolysis of ATP to the reduction of disparate substrates from diatomic gases (Mo and alternative nitrogenases) to photosynthetic pigments (protochlorophyllide and chlorophyllide oxidoreductases). Only very recently have the activities of the highly divergent and paraphyletic Group IV nitrogenases begun to be uncovered. In conclusion, this review highlights the first characterized member of this group, which was found to catalyze an unprecedented reaction in the coenzyme F430 biosynthetic pathway, and the catalytic potential of a superfamily that has yet to be fully explored.
- Publication Date:
- Research Org.:
- Auburn Univ., AL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1656752
- Alternate Identifier(s):
- OSTI ID: 1633690
- Grant/Contract Number:
- SC0018043
- Resource Type:
- Accepted Manuscript
- Journal Name:
- ChemBioChem: a European journal of chemical biology
- Additional Journal Information:
- Journal Volume: 21; Journal Issue: 12; Journal ID: ISSN 1439-4227
- Publisher:
- ChemPubSoc Europe
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Ghebreamlak, Selamawit M., and Mansoorabadi, Steven O.. Divergent Members of the Nitrogenase Superfamily: Tetrapyrrole Biosynthesis and Beyond. United States: N. p., 2020.
Web. https://doi.org/10.1002/cbic.201900782.
Ghebreamlak, Selamawit M., & Mansoorabadi, Steven O.. Divergent Members of the Nitrogenase Superfamily: Tetrapyrrole Biosynthesis and Beyond. United States. https://doi.org/10.1002/cbic.201900782
Ghebreamlak, Selamawit M., and Mansoorabadi, Steven O.. Mon .
"Divergent Members of the Nitrogenase Superfamily: Tetrapyrrole Biosynthesis and Beyond". United States. https://doi.org/10.1002/cbic.201900782. https://www.osti.gov/servlets/purl/1656752.
@article{osti_1656752,
title = {Divergent Members of the Nitrogenase Superfamily: Tetrapyrrole Biosynthesis and Beyond},
author = {Ghebreamlak, Selamawit M. and Mansoorabadi, Steven O.},
abstractNote = {The nitrogenase superfamily constitutes a large and diverse ensemble of two–component metalloenzymes. These systems couple the hydrolysis of ATP to the reduction of disparate substrates from diatomic gases (Mo and alternative nitrogenases) to photosynthetic pigments (protochlorophyllide and chlorophyllide oxidoreductases). Only very recently have the activities of the highly divergent and paraphyletic Group IV nitrogenases begun to be uncovered. In conclusion, this review highlights the first characterized member of this group, which was found to catalyze an unprecedented reaction in the coenzyme F430 biosynthetic pathway, and the catalytic potential of a superfamily that has yet to be fully explored.},
doi = {10.1002/cbic.201900782},
journal = {ChemBioChem: a European journal of chemical biology},
number = 12,
volume = 21,
place = {United States},
year = {2020},
month = {3}
}
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Works referenced in this record:
Distinct structural features of the .alpha. and .beta. subunits of nitrogenase molybdenum-iron protein of Clostridium pasteurianum: an analysis of amino acid sequences
journal, April 1988
- Wang, Shu Zhen; Chen, Jiann Shin; Johnson, John L.
- Biochemistry, Vol. 27, Issue 8
Biological Systems Discovery In Silico: Radical S-Adenosylmethionine Protein Families and Their Target Peptides for Posttranslational Modification
journal, April 2011
- Haft, D. H.; Basu, M. K.
- Journal of Bacteriology, Vol. 193, Issue 11
Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015
- Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8
A Second Nitrogenase-like Enzyme for Bacteriochlorophyll Biosynthesis: RECONSTITUTION OF CHLOROPHYLLIDE a REDUCTASE WITH PURIFIED X-PROTEIN (BchX) AND YZ-PROTEIN (BchY-BchZ) FROM RHODOBACTER CAPSULATUS
journal, March 2006
- Nomata, Jiro; Mizoguchi, Tadashi; Tamiaki, Hitoshi
- Journal of Biological Chemistry, Vol. 281, Issue 21
Nitrogenase MoFe-Protein at 1.16 A Resolution: A Central Ligand in the FeMo-Cofactor
journal, September 2002
- Einsle, O.
- Science, Vol. 297, Issue 5587
Reconstitution of Light-independent Protochlorophyllide Reductase from Purified Bchl and BchN-BchB Subunits
journal, May 2000
- Fujita, Yuichi; Bauer, Carl E.
- Journal of Biological Chemistry, Vol. 275, Issue 31
EPR study of 1Asp-3Cys ligated 4Fe-4S iron-sulfur cluster in NB-protein (BchN-BchB) of a dark-operative protochlorophyllide reductase complex
journal, November 2010
- Kondo, Toru; Nomata, Jiro; Fujita, Yuichi
- FEBS Letters, Vol. 585, Issue 1
Metallophores and Trace Metal Biogeochemistry
journal, November 2014
- Kraemer, Stephan M.; Duckworth, Owen W.; Harrington, James M.
- Aquatic Geochemistry, Vol. 21, Issue 2-4
A pathway for biological methane production using bacterial iron-only nitrogenase
journal, January 2018
- Zheng, Yanning; Harris, Derek F.; Yu, Zheng
- Nature Microbiology, Vol. 3, Issue 3
Erratum: Corrigendum: Elucidation of the biosynthesis of the methane catalyst coenzyme F430
journal, May 2017
- Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher
- Nature, Vol. 545, Issue 7652
Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii
journal, September 1992
- Georgiadis, M.; Komiya, H.; Chakrabarti, P.
- Science, Vol. 257, Issue 5077
Elucidation of the biosynthesis of the methane catalyst coenzyme F430
journal, February 2017
- Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher
- Nature, Vol. 543, Issue 7643
Mo-, V-, and Fe-Nitrogenases Use a Universal Eight-Electron Reductive-Elimination Mechanism To Achieve N 2 Reduction
journal, June 2019
- Harris, Derek F.; Lukoyanov, Dmitriy A.; Kallas, Hayden
- Biochemistry, Vol. 58, Issue 30
Conformational Gating of Electron Transfer from the Nitrogenase Fe Protein to MoFe Protein
journal, May 2010
- Danyal, Karamatullah; Mayweather, Diana; Dean, Dennis R.
- Journal of the American Chemical Society, Vol. 132, Issue 20
Biosynthesis of the Metalloclusters of Molybdenum Nitrogenase
journal, November 2011
- Hu, Y.; Ribbe, M. W.
- Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4
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
journal, July 2001
- Krahn, E.; Weiss, B.; Kröckel, M.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 7, Issue 1-2
Evidence That the P i Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle
journal, June 2016
- Yang, Zhi-Yong; Ledbetter, Rhesa; Shaw, Sudipta
- Biochemistry, Vol. 55, Issue 26
Structure−Function Relationships of Alternative Nitrogenases
journal, January 1996
- Eady, Robert R.
- Chemical Reviews, Vol. 96, Issue 7
The Natural History of Nitrogen Fixation
journal, March 2004
- Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.
- Molecular Biology and Evolution, Vol. 21, Issue 3
Microbial ferric iron reductases
journal, June 2003
- Schröder, Imke; Johnson, Eric; de Vries, Simon
- FEMS Microbiology Reviews, Vol. 27, Issue 2-3
Unique features of the nitrogenase VFe protein from Azotobacter vinelandii
journal, May 2009
- Lee, C. C.; Hu, Y.; Ribbe, M. W.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 23
Differential Reduction of CO 2 by Molybdenum and Vanadium Nitrogenases
journal, September 2014
- Rebelein, Johannes G.; Hu, Yilin; Ribbe, Markus W.
- Angewandte Chemie International Edition, Vol. 53, Issue 43
Construction and characterization of an Azotobacter vinelandii strain with mutations in the genes encoding flavodoxin and ferredoxin I.
journal, June 1989
- Martin, A. E.; Burgess, B. K.; Iismaa, S. E.
- Journal of Bacteriology, Vol. 171, Issue 6
Structural basis of [NiFe] hydrogenase maturation by Hyp proteins
journal, October 2012
- Watanabe, Satoshi; Sasaki, Daisuke; Tominaga, Taiga
- Biological Chemistry, Vol. 393, Issue 10
Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods
journal, March 2001
- Sofia, H. J.
- Nucleic Acids Research, Vol. 29, Issue 5
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea
journal, October 2016
- Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L.
- Science, Vol. 354, Issue 6310
Electron Transfer within Nitrogenase: Evidence for a Deficit-Spending Mechanism
journal, November 2011
- Danyal, Karamatullah; Dean, Dennis R.; Hoffman, Brian M.
- Biochemistry, Vol. 50, Issue 43
In situ click chemistry generation of cyclooxygenase-2 inhibitors
journal, February 2017
- Bhardwaj, Atul; Kaur, Jatinder; Wuest, Melinda
- Nature Communications, Vol. 8, Issue 1
The structure of vanadium nitrogenase reveals an unusual bridging ligand
journal, July 2017
- Sippel, Daniel; Einsle, Oliver
- Nature Chemical Biology, Vol. 13, Issue 9
E ndomicrobium proavitum , the first isolate of E ndomicrobia class. nov. (phylum E lusimicrobia ) - an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase
journal, July 2015
- Zheng, Hao; Dietrich, Carsten; Radek, Renate
- Environmental Microbiology, Vol. 18, Issue 1
The EFI Web Resource for Genomic Enzymology Tools: Leveraging Protein, Genome, and Metagenome Databases to Discover Novel Enzymes and Metabolic Pathways
journal, September 2019
- Zallot, Rémi; Oberg, Nils; Gerlt, John A.
- Biochemistry, Vol. 58, Issue 41
A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase
journal, June 1984
- Simpson, F.; Burris, R.
- Science, Vol. 224, Issue 4653
Microbial pathway for anaerobic 5′-methylthioadenosine metabolism coupled to ethylene formation
journal, November 2017
- North, Justin A.; Miller, Anthony R.; Wildenthal, John A.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 48
X-ray crystal structure of the light-independent protochlorophyllide reductase
journal, May 2010
- Muraki, Norifumi; Nomata, Jiro; Ebata, Kozue
- Nature, Vol. 465, Issue 7294
The Coupling of Electron Transfer in Nitrogenase to the Hydrolysis of Magnesium Adenosine Triphosphate
journal, August 1979
- Thorneley, Roger N. F.; Lowe, David J.; Eday, Robert R.
- Biochemical Society Transactions, Vol. 7, Issue 4
Diversity and complexity of flavodiiron NO/O2 reductases
journal, December 2017
- Folgosa, Filipe; Martins, Maria C.; Teixeira, Miguel
- FEMS Microbiology Letters, Vol. 365, Issue 3
Identification of a nitrogenase FeMo cofactor precursor on NifEN complex
journal, February 2005
- Hu, Y.; Fay, A. W.; Ribbe, M. W.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 9
Stoichiometry, ATP/2e values, and energy requirements for reactions catalyzed by nitrogenase from Azotobacter vinelandii
journal, September 1975
- Watt, Gerald D.; Bulen, William A.; Burns, Andrea
- Biochemistry, Vol. 14, Issue 19
Biosynthesis of coenzyme F430 in methanogenic bacteria. Identification of 15,173-seco-F430-173-acid as an intermediate
journal, December 1987
- Pfaltz, Andreas; Kobelt, Andre; Huster, Rudolf
- European Journal of Biochemistry, Vol. 170, Issue 1-2
X-ray crystal structure of the nitrogenase molybdenum-iron protein from Clostridium pasteurianum at 3.0-.ANG. resolution
journal, July 1993
- Kim, Jongsun; Woo, D.; Rees, D. C.
- Biochemistry, Vol. 32, Issue 28
New Insights into the Biosynthetic Logic of Ribosomally Synthesized and Post-translationally Modified Peptide Natural Products
journal, January 2016
- Ortega, Manuel A.; van der Donk, Wilfred A.
- Cell Chemical Biology, Vol. 23, Issue 1
Expression and Association of Group IV Nitrogenase NifD and NifH Homologs in the Non-Nitrogen-Fixing Archaeon Methanocaldococcus jannaschii
journal, July 2007
- Staples, C. R.; Lahiri, S.; Raymond, J.
- Journal of Bacteriology, Vol. 189, Issue 20
New insights into the evolutionary history of biological nitrogen fixation
journal, January 2013
- Boyd, Eric S.; Peters, John W.
- Frontiers in Microbiology, Vol. 4
Differential Reduction of CO 2 by Molybdenum and Vanadium Nitrogenases
journal, September 2014
- Rebelein, Johannes G.; Hu, Yilin; Ribbe, Markus W.
- Angewandte Chemie, Vol. 126, Issue 43
Crystal Structure of Methyl-Coenzyme M Reductase: The Key Enzyme of Biological Methane Formation
journal, November 1997
- Ermler, U.
- Science, Vol. 278, Issue 5342
Nitrogenase of Klebsiella pneumoniae. Kinetics of the dissociation of oxidized iron protein from molybdenum-iron protein: identification of the rate-limiting step for substrate reduction
journal, November 1983
- Thorneley, R. N. F.; Lowe, D. J.
- Biochemical Journal, Vol. 215, Issue 2
TonB or not TonB: is that the question?This paper is one of a selection of papers published in a Special Issue entitled CSBMCB 53rd Annual Meeting — Membrane Proteins in Health and Disease, and has undergone the Journal’s usual peer review process.
journal, April 2011
- Krewulak, Karla D.; Vogel, Hans J.
- Biochemistry and Cell Biology, Vol. 89, Issue 2
Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle.
journal, June 1978
- Hageman, R. V.; Burris, R. H.
- Proceedings of the National Academy of Sciences, Vol. 75, Issue 6
Mechanism of Mo-Dependent Nitrogenase
journal, June 2009
- Seefeldt, Lance C.; Hoffman, Brian M.; Dean, Dennis R.
- Annual Review of Biochemistry, Vol. 78, Issue 1
Electron transfer precedes ATP hydrolysis during nitrogenase catalysis
journal, September 2013
- Duval, S.; Danyal, K.; Shaw, S.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
‘Democratized’ genomic enzymology web tools for functional assignment
journal, December 2018
- Zallot, Rémi; Oberg, Nils O.; Gerlt, John A.
- Current Opinion in Chemical Biology, Vol. 47
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes
journal, January 2012
- Dos Santos, Patricia C.; Fang, Zhong; Mason, Steven W.
- BMC Genomics, Vol. 13, Issue 1
Crystal structure of a potassium ion transporter, TrkH
journal, February 2011
- Cao, Yu; Jin, Xiangshu; Huang, Hua
- Nature, Vol. 471, Issue 7338
Iron-Sulfur Cluster-dependent Catalysis of Chlorophyllide a Oxidoreductase from Roseobacter denitrificans
journal, November 2014
- Kiesel, Svenja; Wätzlich, Denise; Lange, Christiane
- Journal of Biological Chemistry, Vol. 290, Issue 2
Evidence for Interstitial Carbon in Nitrogenase FeMo Cofactor
journal, November 2011
- Spatzal, T.; Aksoyoglu, M.; Zhang, L.
- Science, Vol. 334, Issue 6058
Genomic Enzymology: Web Tools for Leveraging Protein Family Sequence–Function Space and Genome Context to Discover Novel Functions
journal, August 2017
- Gerlt, John A.
- Biochemistry, Vol. 56, Issue 33
Nitrogenase reduction of carbon-containing compounds
journal, August 2013
- Seefeldt, Lance C.; Yang, Zhi-Yong; Duval, Simon
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Structure of ADP·AIF4–-stabilized nitrogenase complex and its implications for signal transduction
journal, May 1997
- Schindelin, Hermann; Kisker, Caroline; Schlessman, Jamie L.
- Nature, Vol. 387, Issue 6631
Structure and function of the nickel porphinoid, coenzyme F 430 , and of its enzyme, methyl coenzyme M reductase
journal, December 1990
- Friedmann, Herbert C.; Klein, Albrecht; Thauer, Rudolf K.
- FEMS Microbiology Letters, Vol. 87, Issue 3-4
Mechanism of Molybdenum Nitrogenase
journal, January 1996
- Burgess, Barbara K.; Lowe, David J.
- Chemical Reviews, Vol. 96, Issue 7
X-ray Emission Spectroscopy Evidences a Central Carbon in the Nitrogenase Iron-Molybdenum Cofactor
journal, November 2011
- Lancaster, K. M.; Roemelt, M.; Ettenhuber, P.
- Science, Vol. 334, Issue 6058
NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase
journal, March 2006
- Curatti, L.; Ludden, P. W.; Rubio, L. M.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 14
Roles of RubisCO and the RubisCO-Like Protein in 5-Methylthioadenosine Metabolism in the Nonsulfur Purple Bacterium Rhodospirillum rubrum
journal, December 2009
- Singh, J.; Tabita, F. R.
- Journal of Bacteriology, Vol. 192, Issue 5
Molecular Evolution of Nitrogen Fixation: The Evolutionary History of the nifD, nifK, nifE, and nifN Genes
journal, July 2000
- Fani, Renato; Gallo, Romina; Liò, Pietro
- Journal of Molecular Evolution, Vol. 51, Issue 1
Two Biologically Active Ferredoxins from the Aerobic Nitrogen-fixing Bacterium, Azotobacter vinelandii
journal, July 1972
- Yoch, Duane C.; Arnon, Daniel I.
- Journal of Biological Chemistry, Vol. 247, Issue 14
Electron transport to nitrogenase. Purification and characterization of pyruvate:flavodoxin oxidoreductase. The nifJ gene product.
journal, October 1983
- Shah, V. K.; Stacey, G.; Brill, W. J.
- Journal of Biological Chemistry, Vol. 258, Issue 19