A novel enzymatic system against oxidative stress in the thermophilic hydrogen-oxidizing bacterium hydrogenobacter thermophilus

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Sato, Yuya ^a   Kameya, Masafumi ^b   Fushinobu, Shinya ^a   Wakagi, Takayoshi ^a   Arai, Hiroyuki ^a   Ishii, Masaharu ^a   Igarashi, Yasuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOYAMA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FERREDOXIN; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; FERRIPEROXIN; HYDROGEN PEROXIDE; ORGANIC HYDROPEROXIDE; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RUBERYTHRIN; UNCLASSIFIED DRUG; HYDROGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CONFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; FPX GENE; GENE; HYDROGENOBACTER THERMOPHILUS; NONHUMAN; OXIDATIVE STRESS; PHYLOGENETIC TREE; PHYLOGENY; PLASMID; PROTEIN EXPRESSION; THERMOPHILE; THERMOPHILIC BACTERIUM; ULTRAVIOLET SPECTROSCOPY; WILD TYPE; BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL VIABILITY; OXIDATION REDUCTION REACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY;

BACTERIA (MICROORGANISMS); HYDROGENOBACTER THERMOPHILUS;

BACTERIA; BACTERIAL PROTEINS; HYDROGEN; HYDROGEN PEROXIDE; MICROBIAL VIABILITY; MODELS, MOLECULAR; NADP; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDASE; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84859251913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034825     Document Type: Article

References (42)

1. LeGall J, Prickril BC, Moura I, Xavier AV, Moura JJ, et al. (1988) Isolation and characterization of rubrerythrin, a non-heme iron protein from Desulfovibrio vulgaris that contains rubredoxin centers and a hemerythrin-like binuclear iron cluster. Biochemistry 27: 1636-1642.
2. Lehmann Y, Meile L, Teuber M, (1996) Rubrerythrin from Clostridium perfringens: cloning of the gene, purification of the protein, and characterization of its superoxide dismutase function. J Bacteriol 178: 7152-7158.
3. Alban PS, Popham DL, Rippere KE, Krieg NR, (1998) Identification of a gene for a rubrerythrin/nigerythrin-like protein in Spirillum volutans by using amino acid sequence data from mass spectrometry and NH2-terminal sequencing. J Appl Microbiol 85: 875-882.
4. Das A, Coulter ED, Kurtz DM Jr, Ljungdahl LG, (2001) Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidoreductase- rubredoxin and rubrerythrin-type A flavoprotein- high-molecular-weight rubredoxin. J Bacteriol 183: 1560-1567.
5. Sztukowska M, Bugno M, Potempa J, Travis J, Kurtz DM Jr, (2002) Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol 44: 479-488.
6. Weinberg MV, Jenney FE Jr, Cui X, Adams MW, (2004) Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol 186: 7888-7895.
7. Pierik AJ, Wolbert RB, Portier GL, Verhagen MF, Hagen WR, (1993) Nigerythrin and rubrerythrin from Desulfovibrio vulgaris each contain two mononuclear iron centers and two dinuclear iron clusters. Eur J Biochem 212: 237-245.
8. Bonomi F, Kurtz DM, Cui XY, (1996) Ferroxidase activity of recombinant Desulfovibrio vulgaris rubrerythrin. Journal of Biological Inorganic Chemistry 1: 67-72.
9. Coulter ED, Shenvi NV, Kurtz DM, (1999) NADH peroxidase activity of rubrerythrin. Biochemical and Biophysical Research Communications 255: 317-323.
10. Coulter ED, Kurtz DM Jr, (2001) A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reductase. Arch Biochem Biophys 394: 76-86.
11. Kurtz DM Jr, (2006) Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem 100: 679-693.
12. Kawasaki S, Ono M, Watamura Y, Sakai Y, Satoh T, et al. (2007) An O2-inducible rubrerythrin-like protein, rubperoxin, is functional as a H2O2 reductase in an obligatory anaerobe Clostridium acetobutylicum. FEBS Lett 581: 2460-2464.
13. Wakagi T, (2003) Sulerythrin, the smallest member of the rubrerythrin family, from a strictly aerobic and thermoacidophilic archaeon, Sulfolobus tokodaii strain 7. FEMS Microbiol Lett 222: 33-37.
14. Iyer RB, Silaghi-Dumitrescu R, Kurtz DM Jr, Lanzilotta WN, (2005) High-resolution crystal structures of Desulfovibrio vulgaris (Hildenborough) nigerythrin: facile, redox-dependent iron movement, domain interface variability, and peroxidase activity in the rubrerythrins. J Biol Inorg Chem 10: 407-416.
15. Shiba H, Igarashi Y, Kodama T, Minoda Y, (1982) The deficient carbohydrate metabolic pathways and the incomplete tricarboxylic acid cycle in an obligately autotrophic hydrogen-oxidizing bacterium. Agricultural and Biological Chemistry 46: 2341-2345.
16. Pitulle C, Yang Y, Marchiani M, Moore ER, Siefert JL, et al. (1994) Phylogenetic position of the genus Hydrogenobacter. Int J Syst Bacteriol 44: 620-626.
17. Shiba H, Igarashi Y, Kodama T, Minoda Y, (1985) The CO2 assimilation via the reductive tricarboxylic acid cycle in an obligately autotrophic, aerobic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus. Archives of Microbiology 141: 198-203.
18. Schauder R, Widdel F, Fuchs G, (1987) Carbon Assimilation Pathways in Sulfate-Reducing Bacteria II. Enzymes of a Reductive Citric-Acid Cycle in the Autotrophic Desulfobacter-Hydrogenophilus. Archives of Microbiology 148: 218-225.
19. Beh M, Strauss G, Huber R, Stetter KO, Fuchs G, (1993) Enzymes of the Reductive Citric-Acid Cycle in the Autotrophic Eubacterium Aquifex-Pyrophilus and in the Archaebacterium Thermoproteus-Neutrophilus. Archives of Microbiology 160: 306-311.
20. Wahlund TM, Tabita FR, (1997) The reductive tricarboxylic acid cycle of carbon dioxide assimilation: initial studies and purification of ATP-citrate lyase from the green sulfur bacterium Chlorobium tepidum. J Bacteriol 179: 4859-4867.
21. Berg IA, (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77: 1925-1936.
22. Arai H, Kanbe H, Ishii M, Igarashi Y, (2010) Complete genome sequence of the thermophilic, obligately chemolithoautotrophic hydrogen-oxidizing bacterium Hydrogenobacter thermophilus TK-6. J Bacteriol 192: 2651-2652.
23. Fushinobu S, Shoun H, Wakagi T, (2003) Crystal structure of sulerythrin, a rubrerythrin-like protein from a strictly aerobic archaeon, Sulfolobus tokodaii strain 7, shows unexpected domain swapping. Biochemistry 42: 11707-11715.
24. Tempel W, Liu ZJ, Schubot FD, Shah A, Weinberg MV, et al. (2004) Structural genomics of Pyrococcus furiosus: X-ray crystallography reveals 3D domain swapping in rubrerythrin. Proteins 57: 878-882.
25. Zhao W, Ye Z, Zhao J, (2007) RbrA, a cyanobacterial rubrerythrin, functions as a FNR-dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC 7120. Mol Microbiol 66: 1219-1230.
26. Kawasaki S, Sakai Y, Takahashi T, Suzuki I, Niimura Y, (2009) O2 and reactive oxygen species detoxification complex, composed of O2-responsive NADH:rubredoxin oxidoreductase-flavoprotein A2-desulfoferrodoxin operon enzymes, rubperoxin, and rubredoxin, in Clostridium acetobutylicum. Appl Environ Microbiol 75: 1021-1029.
27. McCord JM, Fridovich I, (1969) The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem 244: 6056-6063.
28. Keele BB Jr, McCord JM, Fridovich I, (1970) Superoxide dismutase from Escherichia coli B. A new manganese-containing enzyme. J Biol Chem 245: 6176-6181.
29. Peschek GA, Wastyn M, Trnka M, Molitor V, Fry IV, et al. (1989) Characterization of the cytochrome c oxidase in isolated and purified plasma membranes from the cyanobacterium Anacystis nidulans. Biochemistry 28: 3057-3063.
30. Richter OM, Tao JS, Turba A, Ludwig B, (1994) A cytochrome ba3 functions as a quinol oxidase in Paracoccus denitrificans. Purification, cloning, and sequence comparison. J Biol Chem 269: 23079-23086.
31. Yamamoto M, Arai H, Ishii M, Igarashi Y, (2006) Role of two 2-oxoglutarate:ferredoxin oxidoreductases in Hydrogenobacter thermophilus under aerobic and anaerobic conditions. FEMS Microbiol Lett 263: 189-193.
32. Lanzilotta WN, Dillard BD, Demick JM, Adams MWW, (2011) A cryo-crystallographic time course for peroxide reduction by rubrerythrin from Pyrococcus furiosus. Journal of Biological Inorganic Chemistry 16: 949-959.
33. Kawasaki S, Ishikura J, Watamura Y, Niimura Y, (2004) Identification of O2-induced peptides in an obligatory anaerobe, Clostridium acetobutylicum. FEBS Lett 571: 21-25.
34. Jacob F, (1977) Evolution and tinkering. Science 196: 1161-1166.
35. Andrews SC, (2010) The Ferritin-like superfamily: Evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim Biophys Acta 1800 691-705 pp. 691-705.
36. Cooley RB, Rhoads TW, Arp DJ, Karplus PA, (2011) A diiron protein autogenerates a valine-phenylalanine cross-link. Science 332: 929.
37. Cooley RB, Arp DJ, Karplus PA, (2011) Symerythrin Structures at Atomic Resolution and the Origins of Rubrerythrins and the Ferritin-Like Superfamily. J Mol Biol.
38. Ishii M, Kawasumi T, Igarashi Y, Kodama T, Minoda Y, (1987) 2-Methylthio-1,4-naphthoquinone, a unique sulfur-containing quinone from a thermophilic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus. J Bacteriol 169: 2380-2384.
39. Hoseki J, Yano T, Koyama Y, Kuramitsu S, Kagamiyama H, (1999) Directed evolution of thermostable kanamycin-resistance gene: a convenient selection marker for Thermus thermophilus. J Biochem 126: 951-956.
40. Wolff SP, (1994) Ferrous Ion Oxidation in Presence of Ferric Ion Indicator Xylenol Orange for Measurement of Hydroperoxides. Methods in Enzymology 233: 182-189.
41. Ikeda T, Nakamura M, Arai H, Ishii M, Igarashi Y, (2009) Ferredoxin-NADP reductase from the thermophilic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus TK-6. FEMS Microbiol Lett 297: 124-130.
42. Ukeda H, Maeda S, Ishii T, Sawamura M, (1997) Spectrophotometric assay for superoxide dismutase based on tetrazolium salt 3′-1- (phenylamino)-carbonyl-3, 4-tetrazolium]-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate reduction by xanthine-xanthine oxidase. Anal Biochem 251: 206-209.