Home LiteratureArticle Details
PMID: 8892819 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Characterization of the region encoding the CO-induced hydrogenase of Rhodospirillum rubrum.

Journal of bacteriology ·Vol. 178 ·No. 21 ·1996-11-00 ·Pages 6200-8

Fox JD, He Y, Shelver D, Roberts GP, Ludden PW

Abstract

In the photosynthetic bacterium Rhodospirillum rubrum, the presence of carbon monoxide (CO) induces expression of several proteins. These include carbon monoxide dehydrogenase (CODH) and a CO-tolerant hydrogenase. Together these enzymes catalyze the following conversion: CO + H2O --> CO2 + H2. This system enables R. rubrum to grow in the dark on CO as the sole energy source. Expression of this system has been shown previously to be regulated at the transcriptional level by CO. We have now identified the remainder of the CO-regulated genes encoded in a contiguous region of the R. rubrum genome. These genes, cooMKLXU, apparently encode proteins related to the function of the CO-induced hydrogenase. As seen before with the gene for the large subunit of the CO-induced hydrogenase (cooH), most of the proteins predicted by these additional genes show significant sequence similarity to subunits of Escherichia coli hydrogenase 3. In addition, all of the newly identified coo gene products show similarity to subunits of NADH-quinone oxidoreductase (energy-conserving NADH dehydrogenase I) from various eukaryotic and prokaryotic organisms. We have found that dicyclohexylcarbodiimide, an inhibitor of mitochondrial NADH dehydrogenase I (also called complex I), inhibits the CO-induced hydrogenase as well. We also show that expression of the cooMKLXUH operon is regulated by CO and the transcriptional activator CooA in a manner similar to that of the cooFSCTJ operon that encodes the subunits of CODH and related proteins.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/genetics Base Sequence Carbon Monoxide/pharmacology DNA, Bacterial Deoxyribonuclease I/metabolism Energy Metabolism Hydrogenase/antagonists & inhibitors,genetics Molecular Sequence Data Oxidoreductases/genetics Peroxidases Peroxiredoxins Rhodospirillum rubrum/drug effects,enzymology Sequence Homology, Amino Acid
Chemicals
Bacterial Proteins DNA, Bacterial Carbon Monoxide Oxidoreductases Peroxidases Peroxiredoxins Hydrogenase Deoxyribonuclease I
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Fox J D
Department of Biochemistry, University of Wisconsin-Madison, 53706, USA.
He Y
Shelver D
Roberts G P
Ludden P W
References (52)
52 references, click to expand
  1. Structure of the extracellular ferredoxin from Rhodospirillum rubrum: close similarity to clostridial ferredoxins.
    J Biochem. 1983 May;93(5):1385-90 PMID: 6411697
  2. The structure and mechanism of iron-hydrogenases.
    Biochim Biophys Acta. 1990 Nov 5;1020(2):115-45 PMID: 2173950
  3. Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase.
    Nature. 1985 Apr 18-24;314(6012):592-7 PMID: 3921850
  4. Sequence homologies among mitochondrial DNA-coded URF2, URF4 and URF5.
    FEBS Lett. 1985 Sep 9;189(1):85-8 PMID: 4029400
  5. Coupling of carbon monoxide oxidation to CO2 and H2 with the phosphorylation of ADP in acetate-grown Methanosarcina barkeri.
    Eur J Biochem. 1986 Sep 1;159(2):393-8 PMID: 3093229
  6. Purification and characterization of carbon monoxide dehydrogenase, a nickel, zinc, iron-sulfur protein, from Rhodospirillum rubrum.
    J Biol Chem. 1987 Mar 5;262(7):2980-7 PMID: 3029096
  7. Inhibition of NADH-ubiquinone reductase activity by N,N'-dicyclohexylcarbodiimide and correlation of this inhibition with the occurrence of energy-coupling site 1 in various organisms.
    Biochemistry. 1987 May 19;26(10):2822-8 PMID: 3111526
  8. Membrane topography of anaerobic carbon monoxide oxidation in Rhodocyclus gelatinosus.
    J Bacteriol. 1987 Oct;169(10):4784-9 PMID: 3308854
  9. Microbial hydrogenases: primary structure, classification, signatures and phylogeny.
    FEMS Microbiol Rev. 1993 Apr;10(3-4):243-69 PMID: 8318259
  10. Intimate relationships of the large and the small subunits of all nickel hydrogenases with two nuclear-encoded subunits of mitochondrial NADH: ubiquinone oxidoreductase.
    Biochim Biophys Acta. 1993 Sep 13;1144(2):221-4 PMID: 8369340
  11. The gene locus of the proton-translocating NADH: ubiquinone oxidoreductase in Escherichia coli. Organization of the 14 genes and relationship between the derived proteins and subunits of mitochondrial complex I.
    J Mol Biol. 1993 Sep 5;233(1):109-22 PMID: 7690854
  12. Protein classification by stochastic modeling and optimal filtering of amino-acid sequences.
    Math Biosci. 1994 Jan;119(1):35-75 PMID: 8111135
  13. Nickel hydrogenases: in search of the active site.
    Biochim Biophys Acta. 1994 Dec 30;1188(3):167-204 PMID: 7803444
  14. Characterisation of a protease from Escherichia coli involved in hydrogenase maturation.
    Eur J Biochem. 1995 Jan 15;227(1-2):545-50 PMID: 7851435
  15. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas.
    Nature. 1995 Feb 16;373(6515):580-7 PMID: 7854413
  16. Carbon monoxide-induced activation of gene expression in Rhodospirillum rubrum requires the product of cooA, a member of the cyclic AMP receptor protein family of transcriptional regulators.
    J Bacteriol. 1995 Apr;177(8):2157-63 PMID: 7721706
  17. Carbon monoxide-dependent growth of Rhodospirillum rubrum.
    J Bacteriol. 1995 Apr;177(8):2241-4 PMID: 7721719
  18. Cloning of an organic solvent-resistance gene in Escherichia coli: the unexpected role of alkylhydroperoxide reductase.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7617-21 PMID: 7644465
  19. Characterization of a CO-responsive transcriptional activator from Rhodospirillum rubrum.
    J Biol Chem. 1996 Jan 5;271(1):120-3 PMID: 8550545
  20. Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme.
    J Bacteriol. 1996 Mar;178(6):1515-24 PMID: 8626276
  21. Mitochondrial electron-transport inhibitors.
    Methods Enzymol. 1979;55:454-62 PMID: 223000
  22. Hydrogenase.
    Biochim Biophys Acta. 1980 Dec;594(2-3):105-76 PMID: 6786341
  23. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome.
    J Mol Biol. 1982 Apr 25;156(4):683-717 PMID: 7120390
  24. Cloning, characterization, and sequencing of the genes encoding the large and small subunits of the periplasmic [NiFe]hydrogenase of Desulfovibrio gigas.
    DNA. 1987 Dec;6(6):539-51 PMID: 3322743
  25. Ferredoxin requirement for electron transport from the carbon monoxide dehydrogenase complex to a membrane-bound hydrogenase in acetate-grown Methanosarcina thermophila.
    J Biol Chem. 1988 Mar 25;263(9):4075-9 PMID: 3279028
  26. The structural genes coding for the L and M subunits of Rhodospirillum rubrum photoreaction center.
    J Biol Chem. 1988 Jun 5;263(16):7632-8 PMID: 2836391
  27. Identification of the dicyclohexylcarbodiimide-binding subunit of NADH-ubiquinone oxidoreductase (Complex I).
    J Biol Chem. 1988 Nov 5;263(31):16150-5 PMID: 3141400
  28. Proton translocation coupled to the oxidation of carbon monoxide to CO2 and H2 in Methanosarcina barkeri.
    Eur J Biochem. 1989 Feb 1;179(2):469-72 PMID: 2537211
  29. An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp.
    J Bacteriol. 1989 Apr;171(4):2049-55 PMID: 2649484
  30. Analysis and comparison of nucleotide sequences encoding the genes for [NiFe] and [NiFeSe] hydrogenases from Desulfovibrio gigas and Desulfovibrio baculatus.
    J Bacteriol. 1989 May;171(5):2894-9 PMID: 2651421
  31. Regulation of carbon monoxide dehydrogenase and hydrogenase in Rhodospirillum rubrum: effects of CO and oxygen on synthesis and activity.
    J Bacteriol. 1989 Jun;171(6):3102-7 PMID: 2498285
  32. Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase from Rhodospirillum rubrum.
    Mol Gen Genet. 1989 Aug;218(2):340-7 PMID: 2506427
  33. The product of the Klebsiella pneumoniae nifX gene is a negative regulator of the nitrogen fixation (nif) regulon.
    J Bacteriol. 1990 Mar;172(3):1441-7 PMID: 2155202
  34. Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components.
    Mol Microbiol. 1990 Feb;4(2):231-43 PMID: 2187144
  35. The 30-kilodalton subunit of bovine mitochondrial complex I is homologous to a protein coded in chloroplast DNA.
    Biochemistry. 1991 Feb 19;30(7):1901-8 PMID: 1899621
  36. A homologue of a nuclear-coded iron-sulfur protein subunit of bovine mitochondrial complex I is encoded in chloroplast genomes.
    Biochemistry. 1991 Mar 19;30(11):2954-60 PMID: 1901022
  37. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria.
    Eur J Biochem. 1991 May 8;197(3):563-76 PMID: 2029890
  38. Characterization of the CO oxidation/H2 evolution system of Rhodospirillum rubrum. Role of a 22-kDa iron-sulfur protein in mediating electron transfer between carbon monoxide dehydrogenase and hydrogenase.
    J Biol Chem. 1991 Sep 25;266(27):18395-403 PMID: 1917963
  39. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome.
    J Mol Biol. 1992 Jan 5;223(1):1-7 PMID: 1731062
  40. Structure-function relationships among the nickel-containing hydrogenases.
    FEMS Microbiol Rev. 1992 Feb;8(2):109-35 PMID: 1558764
  41. NADH: ubiquinone oxidoreductase from bovine heart mitochondria. A fourth nuclear encoded subunit with a homologue encoded in chloroplast genomes.
    FEBS Lett. 1992 Apr 27;301(3):237-42 PMID: 1577158
  42. Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli.
    Mol Microbiol. 1992 Jun;6(11):1523-32 PMID: 1625581
  43. Gene cluster of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans: characterization of four structural gene products.
    Biochemistry. 1992 Aug 4;31(30):6925-32 PMID: 1637825
  44. Genetic and physiological characterization of the Rhodospirillum rubrum carbon monoxide dehydrogenase system.
    J Bacteriol. 1992 Aug;174(16):5284-94 PMID: 1644755
  45. Resolution of NADH:ubiquinone oxidoreductase from bovine heart mitochondria into two subcomplexes, one of which contains the redox centers of the enzyme.
    Biochemistry. 1992 Nov 24;31(46):11425-34 PMID: 1332758
  46. The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in Escherichia coli.
    Arch Microbiol. 1992;158(6):444-51 PMID: 1482271
  47. DNA sequencing of the seven remaining structural genes of the gene cluster encoding the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans.
    Biochemistry. 1993 Jan 26;32(3):968-81 PMID: 8422400
  48. Structural analysis based on state-space modeling.
    Protein Sci. 1993 Mar;2(3):305-14 PMID: 8453370
  49. Cotranscriptional expression of mitochondrial genes for subunits of NADH dehydrogenase, nad5, nad4, nad2, in Marchantia polymorpha.
    Mol Gen Genet. 1993 Mar;237(3):343-50 PMID: 8483448
  50. Alkyl hydroperoxide reductase from Salmonella typhimurium. Sequence and homology to thioredoxin reductase and other flavoprotein disulfide oxidoreductases.
    J Biol Chem. 1990 Jun 25;265(18):10535-40 PMID: 2191951
  51. The same domain motif for ubiquinone reduction in mitochondrial or chloroplast NADH dehydrogenase and bacterial glucose dehydrogenase.
    FEBS Lett. 1990 Jun 4;265(1-2):37-40 PMID: 2142103
  52. Association of hydrogen metabolism with unitrophic or mixotrophic growth of Methanosarcina barkeri on carbon monoxide.
    J Bacteriol. 1984 Apr;158(1):373-5 PMID: 6715282
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-11-00
Pages
6200-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC178490
Subset
IM
Databases
GENBANK
U65510
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]