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Role of hydrogen generation by Klebsiella pneumoniae in the oral cavity

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Abstract

Some gastrointestinal bacteria synthesize hydrogen (H2) by fermentation. Despite the presence of bactericidal factors in human saliva, a large number of bacteria also live in the oral cavity. It has never been shown that oral bacteria also produce H2 or what role H2 might play in the oral cavity. It was found that a significant amount of H2 is synthesized in the oral cavity of healthy human subjects, and that its generation is enhanced by the presence of glucose but inhibited by either teeth brushing or sterilization with povidone iodine. These observations suggest the presence of H2-generating bacteria in the oral cavity. The screening of commensal bacteria in the oral cavity revealed that a variety of anaerobic bacteria generate H2. Among them, Klebsiella pneumoniae (K. pneumoniae) generated significantly large amounts of H2 in the presence of glucose. Biochemical analysis revealed that various proteins in K. pneumoniae are carbonylated under standard culture conditions, and that oxidative stress induced by the presence of Fe++ and H2O2 increases the number of carbonylated proteins, particularly when their hydrogenase activity is inhibited by KCN. Inhibition of H2 generation markedly suppresses the growth of K. pneumoniae. These observations suggest that H2 generation and/or the reduction of oxidative stress is important for the survival and growth of K. pneumoniae in the oral cavity.

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References

  • Adams, M.W. 1990. The structure and mechanism of iron-hydrogenases. Biochim. Biophys. Acta. 1020, 115–145.

    Article  CAS  PubMed  Google Scholar 

  • Adams, M.W. and E.I. Stiefel. 1998. Biological hydrogen production: not so elementary. Science 282, 1842–1843.

    Article  CAS  PubMed  Google Scholar 

  • Brondz, I. and I. Olsen. 1986. Chemotaxonomy of selected species of the Actinobacillus-Haemophilus-Pasteurella group by means of gas chromatography, gas chromatography-mass spectrometry and bioenzymatic methods. J. Chromatogr. 380, 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Choudhury, T., E.F. Sato, and M. Inoue. 2007. Nitrite reductase in Streptoccocus mutans plays a critical role in the survival of this pathogen in oral cavity. Oral Microbiol. Immunol. 22, 384–389.

    Article  CAS  PubMed  Google Scholar 

  • De Lacey, A.L., V.M. Fernandez, M. Rousset, and R. Cammack. 2007. Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. Chem. Rev. 107, 4304–4330.

    Article  PubMed  Google Scholar 

  • Fang, H.H., T. Zhang, and C. Li. 2006. Characterization of Fehydrogenase genes diversity and hydrogen-producing population in an acidophilic sludge. J. Biotechnol. 126, 357–364.

    Article  CAS  PubMed  Google Scholar 

  • Fukuda, K., S. Asoh, M. Ishikawa, Y. Yamamoto, I. Ohsawa, and S. Ohta. 2007. Inhalation of hydrogen gas suppresses hepatic injury caused by ischemia/reperfusion through reducing oxidative stress. Biochem. Biophys. Res. Commun. 361, 670–674.

    Article  CAS  PubMed  Google Scholar 

  • Harfoot, C.G. 1978. Lipid metabolism in the rumen. Prog. Lipid Res. 17, 21–54.

    Article  CAS  PubMed  Google Scholar 

  • Hayashida, K., M. Sano, I. Ohsawa, K. Shinmura, K. Tamaki, K. Kimura, J. Endo, and et al. 2008. Inhalation of hydrogen gas reduces infarct size in the rat model of myocardial ischemiareperfusion injury. Biochem. Biophys. Res. Commun. 373, 30–35.

    Article  CAS  PubMed  Google Scholar 

  • Kajiyama, S., G. Hasegawa, M. Asano, H. Hosoda, M. Fukui, N. Nakamura, J. Kitawaki, and et al. 2008. Supplementation of hydrogen-rich water improves lipid and glucose metabolism in patients with type 2 diabetes or impaired glucose tolerance. Nutr. Res. 28, 137–143.

    Article  CAS  PubMed  Google Scholar 

  • Lee, M.R., S.A. Huws, N.D. Scollan, and R.J. Dewhurst. 2007. Effects of fatty acid oxidation products (green odor) on rumen bacterial populations and lipid metabolism in vitro. J. Dairy Sci. 90, 3874–3882.

    Article  CAS  PubMed  Google Scholar 

  • Liu, F. and B.S. Fang. 2007. Cloning and sequence analysis of the gene encoding NiFe-hydrogenase from Klebsiella pneumoniae. Sheng Wu Gong Cheng Xue Bao. 23, 133–137.

    CAS  PubMed  Google Scholar 

  • Lyon, E.J., S. Shima, R. Boecher, R.K. Thauer, F.W. Grevels, E. Bill, W. Roseboom, and S.P. Albracht. 2004. Carbon monoxide as an intrinsic ligand to iron in the active site of the iron-sulfur-clusterfree hydrogenase H2-forming methylenetetrahydromethanopterin dehydrogenase as revealed by infrared spectroscopy. J. Am. Chem. Soc. 126, 14239–14248.

    Article  CAS  PubMed  Google Scholar 

  • Nagata, K., N. Nakashima-Kamimura, T. Mikami, I. Ohsawa, and S. Ohta. 2009. Consumption of molecular hydrogen prevents the stress-induced impairments in hippocampus-dependent learning tasks during chronic physical restraint in mice. Neuropsycho pharmacology 34, 501–508.

    Article  CAS  Google Scholar 

  • Nagata, K., H. Yu, M. Nishikawa, M. Kashiba, A. Nakamura, E.F. Sato, T. Tamura, and M. Inoue. 1998. Helicobacter pylori generates superoxide radicals and modulates nitric oxide metabolism. J. Biol. Chem. 273, 14071–14073.

    Article  CAS  PubMed  Google Scholar 

  • Nakahara, H., E.F. Sato, R. Ishisaka, T. Kanno, T. Yoshioka, T. Yasuda, M. Inoue, and K. Utsumi. 1998. Biochemical properties of human oral polymorphonuclear leukocytes. Free Radic. Res. 28, 485–495.

    Article  CAS  PubMed  Google Scholar 

  • Nakamura, A., A. Park, K. Nagata, E.F. Sato, M. Kashiba, T. Tamura, and M. Inoue. 2000. Oxidative cellular damage associated with transformation of Helicobacter pylori from a bacillary to a coccoid form. Free Radic. Biol. Med. 28, 1611–1618.

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa, T., F.S.E.T. Choudhury, K. Nagata, E. Kasahara, H. Matsui, K. Watanabe, and M. Inoue. 2009. Effect of nitric oxide on the oxygen metabolism and growth of E. faecalis. J. Clin. Biochem. Nutr. 44, 178–184.

    Article  CAS  PubMed  Google Scholar 

  • Ohara-Nemoto, Y., H. Haraga, S. Kimura, and T.K. Nemoto. 2008. Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. J. Med. Microbiol. 57, 95–99.

    Article  CAS  PubMed  Google Scholar 

  • Ohsawa, I., M. Ishikawa, K. Takahashi, M. Watanabe, K. Nishimaki, K. Yamagata, K. Katsura, Y. Katayama, S. Asoh, and S. Ohta. 2007. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat. Med. 13, 688–694.

    Article  CAS  PubMed  Google Scholar 

  • Ohsawa, I., K. Nishimaki, K. Yamagata, M. Ishikawa, and S. Ohta. 2008. Consumption of hydrogen water prevents atherosclerosis in apolipoprotein E knockout mice. Biochem. Biophys. Res. Commun. 377, 1195–1198.

    Article  CAS  PubMed  Google Scholar 

  • Park, A.M., Q. Li, K. Nagata, T. Tamura, K. Shimono, E.F. Sato, and M. Inoue. 2004. Oxygen tension regulates reactive oxygen generation and mutation of Helicobacter pylori. Free Radic. Biol. Med. 36, 1126–1133.

    Article  CAS  PubMed  Google Scholar 

  • Peters, J.W., W.N. Lanzilotta, B.J. Lemon, and L.C. Seefeldt. 1998. Xray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853–1858.

    Article  CAS  PubMed  Google Scholar 

  • Sato, E.F., T. Choudhury, T. Nishikawa, and M. Inoue. 2008. Dynamic aspect of reactive oxygen and nitric oxide in oral cavity. J. Clin. Biochem. Nutr. 42, 8–13.

    Article  CAS  PubMed  Google Scholar 

  • Sato, E.F., M. Higashino, K. Ikeda, R. Wake, M. Matsuo, K. Utsumi, and M. Inoue. 2003. Oxidative stress-induced cell death of human oral neutrophils. Am. J. Physiol. Cell. Physiol. 284, 1048–1053.

    Google Scholar 

  • Schut, G.J. and M.W. Adams. 2009. The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J. Bacteriol. 191, 4451–4457.

    Article  CAS  PubMed  Google Scholar 

  • Smith, D.J., J.M. Anderson, W.F. King, J. van Houte, and M.A. Taubman. 1993. Oral streptococcal colonization of infants. Oral Microbiol. Immunol. 8, 1–4.

    Article  PubMed  Google Scholar 

  • Stephensen, C.B., R.B. Sack, and D.A. Sack. 1987. Comparison of noninvasive breath hydrogen test for gastric acid secretion to standard intubation test in infants and young children. Dig. Dis. Sci. 32, 978–984.

    Article  CAS  PubMed  Google Scholar 

  • Steuber, J., W. Krebs, M. Bott, and P. Dimroth. 1999. A membranebound NAD(P)+-reducing hydrogenase provides reduced pyridine nucleotides during citrate fermentation by Klebsiella pneumoniae. J. Bacteriol. 181, 241–245.

    CAS  PubMed  Google Scholar 

  • Volbeda, A., M.H. Charon, C. Piras, E.C. Hatchikian, M. Frey, and J.C. Fontecilla-Camps. 1995. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373, 580–587.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto, M., K. Saeki, and K. Utsumi. 1991. Isolation of human salivary polymorphonuclear leukocytes and their stimulationcoupled responses. Arch. Biochem. Biophys. 289, 76–82.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, H.W., A.S. McMillan, C. McGrath, L.S. Li, and L.P. Samaranayake. 2008. Oral carriage of yeasts and coliforms in stroke sufferers: a prospective longitudinal study. Oral Dis. 14, 60–66.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry & Molecular Pathology, Osaka City University Medical School, Osaka, 545-8585, Japan

    Tomoko Kanazuru, Eisuke F. Sato, Emiko Kasahara, Mika Jikumaru & Masayasu Inoue

  2. Department of Food and Nutrition, Senri Kinran University, Shita, 565-0873, Japan

    Kumiko Nagata

  3. Department of Applied Biochemistry, Kyoto Prefectural University, Kyoto, 606-8522, Japan

    Tomoko Kanazuru, Hiroshi Matsui & Kunihiko Watanabe

  4. Department of Gastroenterology, Kobe University Medical School, Kobe, 650-0017, Japan

    June Inoue

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  1. Tomoko Kanazuru
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  2. Eisuke F. Sato
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  3. Kumiko Nagata
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  4. Hiroshi Matsui
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  5. Kunihiko Watanabe
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  6. Emiko Kasahara
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  7. Mika Jikumaru
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  8. June Inoue
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  9. Masayasu Inoue
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Correspondence to Eisuke F. Sato.

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Kanazuru, T., Sato, E.F., Nagata, K. et al. Role of hydrogen generation by Klebsiella pneumoniae in the oral cavity. J Microbiol. 48, 778–783 (2010). https://doi.org/10.1007/s12275-010-0149-z

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  • DOI: https://doi.org/10.1007/s12275-010-0149-z

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