1887

Microbiology Society logo

Volume 160, Issue 2

Adaptive response of to normal aerobic and forced oxidative stress conditions Free

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.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.068726-0
2014-02-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/2/340.html?itemId=/content/journal/micro/10.1099/mic.0.068726-0&mimeType=html&fmt=ahah

References

  1. Abràmoff M. D., Magalhães P. J., Ram S. J. ( 2004). Image processing with imageJ. Biophotonics Int 11:36–42
     [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 Res 25:3389–3402 [View Article][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 Microbiol 55:155–162 [View Article][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 Biol 340:783–795 [View Article][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 Res 29:2607–2618 [View Article][PubMed]
     [Google Scholar]
  6. Carlsson J., Kujala U., Edlund M. B. ( 1985). Pyruvate dehydrogenase activity in Streptococcus mutans. . Infect Immun 49:674–678[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 Res 27:4636–4641 [View Article][PubMed]
     [Google Scholar]
  8. Ewing B., Green P. ( 1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194[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 Bacteriol 184:2780–2788 [View Article][PubMed]
     [Google Scholar]
  10. Griffiths-Jones S., Bateman A., Marshall M., Khanna A., Eddy S. R. ( 2003). Rfam: an RNA family database. Nucleic Acids Res 31:439–441 [View Article][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 Microbiol 10:345–351 [View Article]
     [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 Bioeng 90:484–493[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 Res 40:Database issueD306–D312 [View Article][PubMed]
     [Google Scholar]
  14. Ide S., Hayakawa T., Okabe K., Koike M. ( 1967). Lipoamide dehydrogenase from human liver. J Biol Chem 242:54–60[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 Microbiol 48:269–279 [View Article][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 Chem 264:1488–1496[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 Catal 347:1139–1146 [View Article]
     [Google Scholar]
  18. Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M. ( 2004). The KEGG resource for deciphering the genome. Nucleic Acids Res 32:Database issueD277–D280 [View Article][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 Res 19:383–394 [View Article][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 Lett 571:21–25 [View Article][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 Microbiol 71:8442–8450[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 Genet 233:483–486[PubMed] [CrossRef]
     [Google Scholar]
  23. Koyama N., Niimura Y., Kozaki M. ( 1988). Bioenergetic properties of a facultatively anaerobic alkalophile. FEMS Microbiol Lett 49:123–126 [View Article]
     [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 Commun 247:659–662 [View Article][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 Biol 305:567–580 [View Article][PubMed]
     [Google Scholar]
  26. Loewen P. C., Switala J. ( 1987). Multiple catalases in Bacillus subtilis. . J Bacteriol 169:3601–3607[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 Res 25:955–964[PubMed] [CrossRef]
     [Google Scholar]
  29. Magrane M. UniProt Consortium ( 2011). UniProt Knowledgebase: a hub of integrated protein data.. Database (Oxford) 2011:bar009 [View Article][PubMed]
     [Google Scholar]
  30. McCord J. M., Fridovich I. ( 1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055[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 Genet 242:201–208 [View Article][PubMed]
     [Google Scholar]
  32. Mishra S., Imlay J. ( 2012). Why do bacteria use so many enzymes to scavenge hydrogen peroxide. Arch Biochem Biophys 525:145–160 [View Article][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 BISMiS 3:1–18
     [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 Microbiol 138:44–48 [View Article][PubMed]
     [Google Scholar]
  35. Neveling U., Bringer-Meyer S., Sahm H. ( 1998). Gene and subunit organization of bacterial pyruvate dehydrogenase complexes. Biochim Biophys Acta 1385:367–372 [View Article][PubMed]
     [Google Scholar]
  36. Niimura Y., Massey V. ( 1996). Reaction mechanism of Amphibacillus xylanus NADH oxidase/alkyl hydroperoxide reductase flavoprotein. J Biol Chem 271:30459–30464 [View Article][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 Chem 51:2271–2275 [View Article]
     [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 Lett 61:79–84 [View Article]
     [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 Bacteriol 40:297–301 [View Article]
     [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 Bacteriol 175:7945–7950[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 Chem 270:25645–25650 [View Article][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 Bacteriol 182:5046–5051 [View Article][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 Bioeng 84:22–27 [View Article]
     [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 Bacteriol 183:2431–2438 [View Article][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 Chem 269:31418–31423[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 Med 28:108–120 [View Article][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 Biochem 267:6126–6133 [View Article][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 Microbiol 101:903–912 [View Article][PubMed]
     [Google Scholar]
  49. Yamada T., Carlsson J. ( 1975). Regulation of lactate dehydrogenase and change of fermentation products in streptococci. . J Bacteriol 124:55–61[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 Bacteriol 182:3740–3747 [View Article][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 Bacteriol 184:2931–2939 [View Article][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 Bacteriol 186:5997–6002 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.068726-0
Loading
Adaptive response of Amphibacillus xylanus to normal aerobic and forced oxidative stress conditions
Microbiology 160, 340 (2014); https://doi.org/10.1099/mic.0.068726-0
/content/journal/micro/10.1099/mic.0.068726-0
/content/journal/micro/10.1099/mic.0.068726-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error