Posttranslational modification of a vanadium nitrogenase

Heiniger, Erin K.; Harwood, Caroline S.

doi:10.1002/mbo3.265

Title: Posttranslational modification of a vanadium nitrogenase

Journal Article · Fri Jun 19 00:00:00 EDT 2015 · MicrobiologyOpen

DOI:https://doi.org/10.1002/mbo3.265· OSTI ID:1623573

Heiniger, Erin K. ^[1]; Harwood, Caroline S. ^[1]

Department of Microbiology, University of Washington, Seattle Washington 98195

In microbes that fix nitrogen, nitrogenase catalyzes the conversion of N₂ to ammonia in an ATP-demanding reaction. To help conserve energy some bacteria inhibit nitrogenase activity upon exposure to ammonium. The purple nonsulfur phototrophic bacterium Rhodopseudomonas palustris strain CGA009 can synthesize three functional nitrogenase isoenzymes: a molybdenum nitrogenase, a vanadium nitrogenase, and an iron nitrogenase. Previous studies showed that in some alphaproteobacteria, including R. palustris, molybdenum nitrogenase activity is inhibited by ADP-ribosylation when cells are exposed to ammonium. Some iron nitrogenases are also post-translationally modified. However, the posttranslational modification of vanadium nitrogenase has not been reported. Here, we investigated the regulation of the alternative nitrogenases of R. palustris and determined that both its vanadium nitrogenase and its iron nitrogenase activities were inhibited and post-translationally modified when cells are exposed to ammonium. Vanadium nitrogenase is not found in all strains of R. palustris, suggesting that it may have been acquired by horizontal gene transfer. Also, phylogenetic analyses of the three nitrogenases suggest that VnfH, the target of ADP-ribosylation, may be the product of a gene duplication of nifH, the molybdenum nitrogenase homolog.

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Research Organization:: Univ. of Washington, Seattle, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-05ER15707

OSTI ID:: 1623573

Journal Information:: MicrobiologyOpen, Vol. 4, Issue 4; ISSN 2045-8827

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (32)

Dissimilatory Reduction of Fe(III) and Other Electron Acceptors by a Thermus Isolate Kieft, T. L.; Fredrickson, J. K.; Onstott, T. C. Applied and Environmental Microbiology, Vol. 65, Issue 3 https://doi.org/10.1128/AEM.65.3.1214-1221.1999	journal	March 1999
Covalent modification of the iron protein of nitrogenase from Rhodospirillum rubrum by adenosine diphosphoribosylation of a specific arginine residue. Pope, M. R.; Murrell, S. A.; Ludden, P. W. Proceedings of the National Academy of Sciences, Vol. 82, Issue 10 https://doi.org/10.1073/pnas.82.10.3173	journal	May 1985
In Vitro Synthesis of the Iron-Molybdenum Cofactor and Maturation of the nif -encoded Apodinitrogenase: EFFECT OF SUBSTITUTION OF VNFH FOR NIFH Chatterjee, Ranjini; Allen, Ronda M.; Ludden, Paul W. Journal of Biological Chemistry, Vol. 272, Issue 34 https://doi.org/10.1074/jbc.272.34.21604	journal	August 1997
Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Harwood, C. S.; Gibson, J. Applied and Environmental Microbiology, Vol. 54, Issue 3 https://doi.org/10.1128/aem.54.3.712-717.1988	journal	January 1988
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Reversible regulation of the nitrogenase iron protein from Rhodospirillum rubrum by ADP-ribosylation in vitro. Lowery, R. G.; Saari, L. L.; Ludden, P. W. Journal of Bacteriology, Vol. 166, Issue 2 https://doi.org/10.1128/jb.166.2.513-518.1986	journal	January 1986
Production of Hydrogen Gas from Light and the Inorganic Electron Donor Thiosulfate by Rhodopseudomonas palustris Huang, J. J.; Heiniger, E. K.; McKinlay, J. B. Applied and Environmental Microbiology, Vol. 76, Issue 23 https://doi.org/10.1128/AEM.01143-10	journal	October 2010
Photobiological production of hydrogen gas as a biofuel McKinlay, James B.; Harwood, Caroline S. Current Opinion in Biotechnology, Vol. 21, Issue 3 https://doi.org/10.1016/j.copbio.2010.02.012	journal	June 2010
Structure−Function Relationships of Alternative Nitrogenases Eady, Robert R. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950057h	journal	January 1996
Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments Oda, Y.; Larimer, F. W.; Chain, P. S. G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 47 https://doi.org/10.1073/pnas.0809160105	journal	November 2008
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
Isolation of a new vanadium-containing nitrogenase from Azotobacter vinelandii Hales, Brian J.; Case, Ellen E.; Morningstar, Joyce E. Biochemistry, Vol. 25, Issue 23 https://doi.org/10.1021/bi00371a001	journal	November 1986
GenBank Benson, D. A.; Karsch-Mizrachi, I.; Clark, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1202	journal	December 2011
Photofermentative hydrogen production from wastes Keskin, Tugba; Abo-Hashesh, Mona; Hallenbeck, Patrick C. Bioresource Technology, Vol. 102, Issue 18 https://doi.org/10.1016/j.biortech.2011.04.004	journal	September 2011
Acetate as a carbon source for hydrogen production by photosynthetic bacteria Barbosa, Maria J.; Rocha, Jorge M. S.; Tramper, Johannes Journal of Biotechnology, Vol. 85, Issue 1 https://doi.org/10.1016/S0168-1656(00)00368-0	journal	January 2001
Role of the Dinitrogenase Reductase Arginine 101 Residue in Dinitrogenase Reductase ADP-Ribosyltransferase Binding, NAD Binding, and Cleavage Ma, Yan; Ludden, Paul W. Journal of Bacteriology, Vol. 183, Issue 1 https://doi.org/10.1128/jb.183.1.250-256.2001	journal	January 2001
Benzoyl Coenzyme A Pathway-Mediated Metabolism of meta-Hydroxy-Aromatic Acids in Rhodopseudomonas palustris Gall, D. L.; Ralph, J.; Donohue, T. J. Journal of Bacteriology, Vol. 195, Issue 18 https://doi.org/10.1128/jb.00634-13	journal	July 2013
Functional Genomic Analysis of Three Nitrogenase Isozymes in the Photosynthetic Bacterium Rhodopseudomonas palustris Oda, Y.; Samanta, S. K.; Rey, F. E. Journal of Bacteriology, Vol. 187, Issue 22 https://doi.org/10.1128/JB.187.22.7784-7794.2005	journal	November 2005
Nitrogen Fixation: The Mechanism of the Mo-Dependent Nitrogenase Igarashi, Robert Y.; Seefeldt, Lance C. Critical Reviews in Biochemistry and Molecular Biology, Vol. 38, Issue 4 https://doi.org/10.1080/10409230391036766	journal	January 2003
Confidence Limits on Phylogenies: an Approach Using the Bootstrap Felsenstein, Joseph Evolution, Vol. 39, Issue 4 https://doi.org/10.1111/j.1558-5646.1985.tb00420.x	journal	July 1985
Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Bishop, P. E.; Jarlenski, D. M.; Hetherington, D. R. Proceedings of the National Academy of Sciences, Vol. 77, Issue 12 https://doi.org/10.1073/pnas.77.12.7342	journal	December 1980
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
How Posttranslational Modification of Nitrogenase Is Circumvented in Rhodopseudomonas palustris Strains That Produce Hydrogen Gas Constitutively Heiniger, Erin K.; Oda, Yasuhiro; Samanta, Sudip K. Applied and Environmental Microbiology, Vol. 78, Issue 4 https://doi.org/10.1128/aem.07254-11	journal	December 2011
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Molybdenum and vanadium nitrogenases of Azotobacter chroococcum. Low temperature favours N2 reduction by vanadium nitrogenase Miller, R. W.; Eady, R. R. Biochemical Journal, Vol. 256, Issue 2 https://doi.org/10.1042/bj2560429	journal	December 1988
Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris Kim, Min-Kyung; Harwood, Caroline S. FEMS Microbiology Letters, Vol. 83, Issue 2 https://doi.org/10.1111/j.1574-6968.1991.tb04440.x-i1	journal	October 1991
Genetic regulation of biological nitrogen fixation Dixon, Ray; Kahn, Daniel Nature Reviews Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nrmicro954	journal	August 2004
The draTG gene region of Rhodobacter capsulatus is required for post-translational regulation of both the molybdenum and the alternative nitrogenase Masepohl, B.; Krey, R.; Klipp, W. Journal of General Microbiology, Vol. 139, Issue 11 https://doi.org/10.1099/00221287-139-11-2667	journal	November 1993
Characterization of anf genes specific for the alternative nitrogenase and identification of nif genes required for both nitrogenases in Rhodobacter capsulatus Schüddekopf, Kerstin; Hennecke, Silke; Liese, Ute Molecular Microbiology, Vol. 8, Issue 4 https://doi.org/10.1111/j.1365-2958.1993.tb01611.x	journal	May 1993
The neighbor-joining method: a new method for reconstructing phylogenetic trees. Saitou, N.; Nei, M. Molecular Biology and Evolution, Vol. 4, Issue 4, p. 406-425 https://doi.org/10.1093/oxfordjournals.molbev.a040454	journal	July 1987
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
Nitrogenases Burris, R. H. Journal of Biological Chemistry, Vol. 266, Issue 15 https://doi.org/10.1016/S0021-9258(18)92821-8	journal	May 1991

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