1887

Abstract

grows at the same rate and with the same cell yield under aerobic and anaerobic conditions. Under aerobic conditions, it exhibits vigorous oxygen consumption in spite of lacking a respiratory system and haem catalase. To understand the adaptive response of . to oxidative stresses, a genomic analysis of was conducted. The analysis showed that has the genes of four metabolic systems: two pyruvate metabolic pathways, a glycolytic metabolic pathway and an NADH oxidase (Nox)–AhpC (Prx) system. A transcriptional study confirmed that has these metabolic systems. Moreover, genomic analysis revealed the presence of two genes for NADH oxidase ( and ), both of which were identified in the transcriptional analysis. The gene in was highly expressed under normal aerobic conditions but that of was not. A purification study of NADH oxidases indicated that the gene product of is a primary metabolic enzyme responsible for metabolism of both oxygen and reactive oxygen species. was successfully grown under forced oxidative stress conditions such as 0.1 mM HO, 0.3 mM paraquat and 80 % oxygen. Proteomic analysis revealed that manganese SOD, Prx, pyruvate dehydrogenase complex E1 and E3 components, and riboflavin synthase β-chain are induced under normal aerobic conditions, and the other proteins except the five aerobically induced proteins were not induced under forced oxidative stress conditions. Taken together, the present findings indicate that has a unique defence system against forced oxidative stress.

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2014-02-01
2020-01-28
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References

  1. Abràmoff M. D., Magalhães P. J., Ram S. J.. ( 2004;). Image processing with imageJ. Biophotonics Int11:36–42
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. ( 1997;). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  3. Arai T., Yanahashi S., Sato J., Sato T., Ishikawa M., Koizumi Y., Kawasaki S., Niimura Y., Nakagawa J.. ( 2009;). Taxonomical and physiological comparisons of the three species of the genus Amphibacillus. . J Gen Appl Microbiol55:155–162 [CrossRef][PubMed]
    [Google Scholar]
  4. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S.. ( 2004;). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol340:783–795 [CrossRef][PubMed]
    [Google Scholar]
  5. Besemer J., Lomsadze A., Borodovsky M.. ( 2001;). GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res29:2607–2618 [CrossRef][PubMed]
    [Google Scholar]
  6. Carlsson J., Kujala U., Edlund M. B.. ( 1985;). Pyruvate dehydrogenase activity in Streptococcus mutans. . Infect Immun49:674–678[PubMed]
    [Google Scholar]
  7. Delcher A. L., Harmon D., Kasif S., White O., Salzberg S. L.. ( 1999;). Improved microbial gene identification with GLIMMER. Nucleic Acids Res27:4636–4641 [CrossRef][PubMed]
    [Google Scholar]
  8. Ewing B., Green P.. ( 1998;). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res8:186–194[PubMed][CrossRef]
    [Google Scholar]
  9. Gao H., Jiang X., Pogliano K., Aronson A. I.. ( 2002;). The E1beta and E2 subunits of the Bacillus subtilis pyruvate dehydrogenase complex are involved in regulation of sporulation. J Bacteriol184:2780–2788 [CrossRef][PubMed]
    [Google Scholar]
  10. Griffiths-Jones S., Bateman A., Marshall M., Khanna A., Eddy S. R.. ( 2003;). Rfam: an RNA family database. Nucleic Acids Res31:439–441 [CrossRef][PubMed]
    [Google Scholar]
  11. Hannsson L., Häggström M. H.. ( 1984;). Effects of growth conditions on the activities of superoxide dismutase and NADH-oxidase/NADH-peroxidase in Streptococcus lactis. . Curr Microbiol10:345–351 [CrossRef]
    [Google Scholar]
  12. Higuchi M., Yamamoto Y., Kamio Y.. ( 2000;). Molecular biology of oxygen tolerance in lactic acid bacteria: Functions of NADH oxidases and Dpr in oxidative stress. J Biosci Bioeng90:484–493[PubMed][CrossRef]
    [Google Scholar]
  13. Hunter S., Jones P., Mitchell A., Apweiler R., Attwood T. K., Bateman A., Bernard T., Binns D., Bork P.. & other authors ( 2012;). InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res40:Database issueD306–D312 [CrossRef][PubMed]
    [Google Scholar]
  14. Ide S., Hayakawa T., Okabe K., Koike M.. ( 1967;). Lipoamide dehydrogenase from human liver. J Biol Chem242:54–60[PubMed]
    [Google Scholar]
  15. Ishikawa M., Ishizaki S., Yamamoto Y., Yamasato K.. ( 2002;). Paraliobacillus ryukyuensis gen. nov., sp. nov., a new Gram-positive, slightly halophilic, extremely halotolerant, facultative anaerobe isolated from a decomposing marine alga. J Gen Appl Microbiol48:269–279 [CrossRef][PubMed]
    [Google Scholar]
  16. Jacobson F. S., Morgan R. W., Christman M. F., Ames B. N.. ( 1989;). An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. Purification and properties. J Biol Chem264:1488–1496[PubMed]
    [Google Scholar]
  17. Jiang R. R., Riebel B. R., Bommarius A. S.. ( 2005;). Comparison of alkyl hydroperoxide reductase (AhpR) and water-forming NADH oxidase from Lactococcus lactis ATCC 19435. Adv Synth Catal347:1139–1146 [CrossRef]
    [Google Scholar]
  18. Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M.. ( 2004;). The KEGG resource for deciphering the genome. Nucleic Acids Res32:Database issueD277–D280 [CrossRef][PubMed]
    [Google Scholar]
  19. Kawakoshi A., Nakazawa H., Fukada J., Sasagawa M., Katano Y., Nakamura S., Hosoyama A., Sasaki H., Ichikawa N.. & other authors ( 2012;). Deciphering the genome of polyphosphate accumulating actinobacterium Microlunatus phosphovorus. DNA Res19:383–394 [CrossRef][PubMed]
    [Google Scholar]
  20. Kawasaki S., Ishikura J., Watamura Y., Niimura Y.. ( 2004;). Identification of O2-induced peptides in an obligatory anaerobe, Clostridium acetobutylicum. . FEBS Lett571:21–25 [CrossRef][PubMed]
    [Google Scholar]
  21. Kawasaki S., Watamura Y., Ono M., Watanabe T., Takeda K., Niimura Y.. ( 2005;). Adaptive responses to oxygen stress in obligatory anaerobes Clostridium acetobutylicum and Clostridium aminovalericum . Appl Environ Microbiol71:8442–8450[PubMed][CrossRef]
    [Google Scholar]
  22. Kil Y. V., Mironov V. N., Gorishin IYu, Kreneva R. A., Perumov D. A.. ( 1992;). Riboflavin operon of Bacillus subtilis: unusual symmetric arrangement of the regulatory region. Mol Gen Genet233:483–486[PubMed][CrossRef]
    [Google Scholar]
  23. Koyama N., Niimura Y., Kozaki M.. ( 1988;). Bioenergetic properties of a facultatively anaerobic alkalophile. FEMS Microbiol Lett49:123–126 [CrossRef]
    [Google Scholar]
  24. Koyama N., Koitabashi T., Niimura Y., Massey V.. ( 1998;). Peroxide reductase activity of NADH dehydrogenase of an alkaliphilic Bacillus in the presence of a 22-kDa protein component from Amphibacillus xylanus. . Biochem Biophys Res Commun247:659–662 [CrossRef][PubMed]
    [Google Scholar]
  25. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L.. ( 2001;). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol305:567–580 [CrossRef][PubMed]
    [Google Scholar]
  26. Loewen P. C., Switala J.. ( 1987;). Multiple catalases in Bacillus subtilis. . J Bacteriol169:3601–3607[PubMed]
    [Google Scholar]
  27. Logan N. A., Vos P. D.. ( 2009;). Genus I. Bacillus Cohn 1872, 174AL.. Bergey’s Manual of Systematic Bacteriology21–128 De Vos P., Garrity G. M., Jones D., Krieg N. R., Ludwig W., Rainey F. A., Schleifer K.-H., Whitman W. B.. New York: Springer;
    [Google Scholar]
  28. Lowe T. M., Eddy S. R.. ( 1997;). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res25:955–964[PubMed][CrossRef]
    [Google Scholar]
  29. Magrane M.. UniProt Consortium ( 2011;). UniProt Knowledgebase: a hub of integrated protein data.. Database (Oxford)2011:bar009 [CrossRef][PubMed]
    [Google Scholar]
  30. McCord J. M., Fridovich I.. ( 1969;). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem244:6049–6055[PubMed]
    [Google Scholar]
  31. Mironov V. N., Kraev A. S., Chikindas M. L., Chernov B. K., Stepanov A. I., Skryabin K. G.. ( 1994;). Functional organization of the riboflavin biosynthesis operon from Bacillus subtilis SHgw. Mol Gen Genet242:201–208 [CrossRef][PubMed]
    [Google Scholar]
  32. Mishra S., Imlay J.. ( 2012;). Why do bacteria use so many enzymes to scavenge hydrogen peroxide. Arch Biochem Biophys525:145–160 [CrossRef][PubMed]
    [Google Scholar]
  33. Mochizuki D., Tanaka N., Ishikawa M., Endo K., Shiwa Y., Fujita N., Sato J., Niimura Y.. ( 2012;). Evolution and diversification of oxygen metabolisms of aerotolerant anaerobes in the order Bacillales and other bacterial taxonomic groups. The Bulletin of BISMiS3:1–18
    [Google Scholar]
  34. Murphy M. G., Condon S.. ( 1984;). Correlation of oxygen utilization and hydrogen peroxide accumulation with oxygen induced enzymes in Lactobacillus plantarum cultures. Arch Microbiol138:44–48 [CrossRef][PubMed]
    [Google Scholar]
  35. Neveling U., Bringer-Meyer S., Sahm H.. ( 1998;). Gene and subunit organization of bacterial pyruvate dehydrogenase complexes. Biochim Biophys Acta1385:367–372 [CrossRef][PubMed]
    [Google Scholar]
  36. Niimura Y., Massey V.. ( 1996;). Reaction mechanism of Amphibacillus xylanus NADH oxidase/alkyl hydroperoxide reductase flavoprotein. J Biol Chem271:30459–30464 [CrossRef][PubMed]
    [Google Scholar]
  37. Niimura Y., Yanagida F., Uchimura T., Ohara N., Suzuki K., Kozaki M.. ( 1987;). A new facultative anaerobic xylan-using alkalophile lacking cytochrome, quinone, and catalase. Agric Biol Chem51:2271–2275 [CrossRef]
    [Google Scholar]
  38. Niimura Y., Koh E., Uchimura T., Ohara N., Kozaki M.. ( 1989;). Aerobic and anaerobic metabolism in a facultative anaerobe Ep01 lacking cytochrome, quinone and catalase. FEMS Microbiol Lett61:79–84 [CrossRef]
    [Google Scholar]
  39. Niimura Y., Koh E., Yanagida F., Suzuki K. I., Komagata K., Kozaki M.. ( 1990;). Amphibacillus xylanus gen-nov, sp-nov, a facultatively anaerobic spore-forming xylan-digesting bacterium which lacks cytochrome, quinone, and catalase. Int J Syst Bacteriol40:297–301 [CrossRef]
    [Google Scholar]
  40. Niimura Y., Ohnishi K., Yarita Y., Hidaka M., Masaki H., Uchimura T., Suzuki H., Kozaki M., Uozumi T.. ( 1993;). A flavoprotein functional as NADH oxidase from Amphibacillus xylanus Ep01: purification and characterization of the enzyme and structural analysis of its gene. J Bacteriol175:7945–7950[PubMed]
    [Google Scholar]
  41. Niimura Y., Poole L. B., Massey V.. ( 1995;). Amphibacillus xylanus NADH oxidase and Salmonella typhimurium alkyl-hydroperoxide reductase flavoprotein components show extremely high scavenging activity for both alkyl hydroperoxide and hydrogen peroxide in the presence of S. typhimurium alkyl-hydroperoxide reductase 22-kDa protein component. J Biol Chem270:25645–25650 [CrossRef][PubMed]
    [Google Scholar]
  42. Niimura Y., Nishiyama Y., Saito D., Tsuji H., Hidaka M., Miyaji T., Watanabe T., Massey V.. ( 2000;). A hydrogen peroxide-forming NADH oxidase that functions as an alkyl hydroperoxide reductase in Amphibacillus xylanus. . J Bacteriol182:5046–5051 [CrossRef][PubMed]
    [Google Scholar]
  43. Nishiyama Y., Massey V., Anzai Y., Watanabe T., Miyaji T., Uchimura T., Kozaki M., Suzuki H., Niimura Y.. ( 1997;). Purification and characterization of Sporolactobacillus inulinus NADH oxidase and its physiological role in aerobic metabolism of the bacterium. J Ferment Bioeng84:22–27 [CrossRef]
    [Google Scholar]
  44. Nishiyama Y., Massey V., Takeda K., Kawasaki S., Sato J., Watanabe T., Niimura Y.. ( 2001;). Hydrogen peroxide-forming NADH oxidase belonging to the peroxiredoxin oxidoreductase family: existence and physiological role in bacteria. J Bacteriol183:2431–2438 [CrossRef][PubMed]
    [Google Scholar]
  45. Ohnishi K., Niimura Y., Yokoyama K., Hidaka M., Masaki H., Uchimura T., Suzuki H., Uozumi T., Kozaki M.. & other authors ( 1994;). Purification and analysis of a flavoprotein functional as NADH oxidase from Amphibacillus xylanus overexpressed in Escherichia coli . J Biol Chem269:31418–31423[PubMed]
    [Google Scholar]
  46. Poole L. B., Higuchi M., Shimada M., Calzi M. L., Kamio Y.. ( 2000a;). Streptococcus mutans H2O2-forming NADH oxidase is an alkyl hydroperoxide reductase protein. Free Radic Biol Med28:108–120 [CrossRef][PubMed]
    [Google Scholar]
  47. Poole L. B., Reynolds C. M., Wood Z. A., Karplus P. A., Ellis H. R., Li Calzi M.. ( 2000b;). AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur J Biochem267:6126–6133 [CrossRef][PubMed]
    [Google Scholar]
  48. Quatravaux S., Remize F., Bryckaert E., Colavizza D., Guzzo J.. ( 2006;). Examination of Lactobacillus plantarum lactate metabolism side effects in relation to the modulation of aeration parameters. J Appl Microbiol101:903–912 [CrossRef][PubMed]
    [Google Scholar]
  49. Yamada T., Carlsson J.. ( 1975;). Regulation of lactate dehydrogenase and change of fermentation products in streptococci. . J Bacteriol124:55–61[PubMed]
    [Google Scholar]
  50. Yamamoto Y., Higuchi M., Poole L. B., Kamio Y.. ( 2000;). Role of the dpr product in oxygen tolerance in Streptococcus mutans. . J Bacteriol182:3740–3747 [CrossRef][PubMed]
    [Google Scholar]
  51. Yamamoto Y., Poole L. B., Hantgan R. R., Kamio Y.. ( 2002;). An iron-binding protein, Dpr, from Streptococcus mutans prevents iron-dependent hydroxyl radical formation in vitro. J Bacteriol184:2931–2939 [CrossRef][PubMed]
    [Google Scholar]
  52. Yamamoto Y., Fukui K., Koujin N., Ohya H., Kimura K., Kamio Y.. ( 2004;). Regulation of the intracellular free iron pool by Dpr provides oxygen tolerance to Streptococcus mutans. . J Bacteriol186:5997–6002 [CrossRef][PubMed]
    [Google Scholar]
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