Advertisement

Journal of Microbiology

, Volume 56, Issue 4, pp 238–245 | Cite as

Hydrogen sulfide inhibits the growth of Escherichia coli through oxidative damage

  • Liu-Hui Fu
  • Zeng-Zheng Wei
  • Kang-Di Hu
  • Lan-Ying Hu
  • Yan-Hong Li
  • Xiao-Yan Chen
  • Zhuo Han
  • Gai-Fang Yao
  • Hua Zhang
Microbial Physiology and Biochemistry

Abstract

Many studies have shown that hydrogen sulfide (H2S) is both detrimental and beneficial to animals and plants, whereas its effect on bacteria is not fully understood. Here, we report that H2S, released by sodium hydrosulfide (NaHS), significantly inhibits the growth of Escherichia coli in a dose-dependent manner. Further studies have shown that H2S treatment stimulates the production of reactive oxygen species (ROS) and decreases glutathione (GSH) levels in E. coli, resulting in lipid peroxidation and DNA damage. H2S also inhibits the antioxidative enzyme activities of superoxide dismutase (SOD), catalase (CAT) and glutathione reductase (GR) and induces the response of the SoxRS and OxyR regulons in E. coli. Moreover, pretreatment with the antioxidant ascorbic acid (AsA) could effectively prevent H2S-induced toxicity in E. coli. Taken together, our results indicate that H2S exhibits an antibacterial effect on E. coli through oxidative damage and suggest a possible application for H2S in water and food processing.

Keywords

hydrogen sulfide Escherichia coli oxidative stress DNA damage antioxidative enzyme 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aroca, Á., Serna, A., Gotor, C., and Romero, L.C. 2015. S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol. 168, 334–342.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Attene-Ramos, M.S., Wagner, E.D., Gaskins, H.R., and Plewa, M.J. 2007. Hydrogen sulfide induces direct radical-associated DNA damage. Mol. Cancer Res. 5, 455–459.CrossRefPubMedGoogle Scholar
  3. Beauchamp, R.O. Jr., Bus, J.S., Popp, J.A., Boreiko, C.J., and Andjelkovich, D.A. 1984. A critical review of the literature on hydrogen sulfide toxicity. Crit. Rev. Toxicol. 13, 25–97.PubMedGoogle Scholar
  4. Borecký, J., Maia, I.G., Costa, A.D., Ježek, P., Chaimovich, H., de Andrade, P.B., Vercesi, A.E., and Arruda, P. 2001. Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUMP1) expressed in Escherichia coli. FEBS Lett. 505, 240–244.CrossRefPubMedGoogle Scholar
  5. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.CrossRefPubMedGoogle Scholar
  6. Cabiscol, E., Tamarit, J., and Ros, J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3, 3–8.PubMedGoogle Scholar
  7. Calderwood, A. and Kopriva, S. 2014. Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41, 72–78.CrossRefPubMedGoogle Scholar
  8. Deng, D., Zhang, N., Mustapha, A., Xu, D., Wuliji, T., Farley, M., Yang, J., Hua, B., Liu, F., and Zheng, G. 2014. Differentiating enteric Escherichia coli from environmental bacteria through the putative glucosyltransferase gene (ycjM). Water Res. 61, 224–231.CrossRefPubMedGoogle Scholar
  9. Eghbal, M.A., Pennefather, P.S., and O’Brien, P.J. 2004. H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203, 69–76.CrossRefPubMedGoogle Scholar
  10. Fang, F.C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99, 2818–2825.PubMedGoogle Scholar
  11. Fu, L.H., Hu, K.D., Hu, L.Y., Li, Y.H., Hu, L.B., Yan, H., Liu, Y.S., and Zhang, H. 2014. An antifungal role of hydrogen sulfide on the postharvest pathogens Aspergillus niger and Penicillium italicum. PLoS One 9, e104206.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Giannopolitis, C.N. and Ries, S.K. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 59, 309–314.PubMedGoogle Scholar
  13. Gusarov, I., Shatalin, K., Starodubtseva, M., and Nudler, E. 2009. Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325, 1380–1384.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hancock, J.T. and Whiteman, M. 2014. Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol. Biochem. 78, 37–42.Google Scholar
  15. Hu, L.Y., Hu, S.L., Wu, J., Li, Y.H., Zheng, J.L., Wei, Z.J., Liu, J., Wang, H.L., Liu, Y.S., and Zhang, H. 2012. Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J. Agric. Food Chem. 60, 8684–8693.CrossRefPubMedGoogle Scholar
  16. Imlay, J.A. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77, 755–776.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Joshi, S.G., Cooper, M., Yost, A., Paff, M., Ercan, U.K., Fridman, G., Friedman, G., Fridman, A., and Brooks, A.D. 2011. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob. Agents Chemother. 55, 1053–1062.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Joyner-Matos, J., Predmore, B.L., Stein, J.R., Leeuwenburgh, C., and Julian, D. 2010. Hydrogen sulfide induces oxidative damage to RNA and DNA in a sulfide-tolerant marine invertebrate. Physiol. Biochem. Zool. 83, 356–365.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ju, Y., Zhang, W., Pei, Y., and Yang, G. 2013. H2S signaling in redox regulation of cellular functions. Can. J. Physiol. Pharmacol. 91, 8–14.CrossRefPubMedGoogle Scholar
  20. Jung, D., Cho, Y., Meyer, J.N., and Di Giulio, R.T. 2009. The long amplicon quantitative PCR for DNA damage assay as a sensitive method of assessing DNA damage in the environmental model, Atlantic killifish (Fundulus heteroclitus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 182–186.CrossRefPubMedGoogle Scholar
  21. Kimura, H. 2011. Hydrogen sulfide: its production, release and functions. Amino Acids 41, 113–121.CrossRefPubMedGoogle Scholar
  22. Kimura, Y., Goto, Y.I., and Kimura, H. 2010. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox. Signal. 12, 1–13.CrossRefPubMedGoogle Scholar
  23. Kimura, Y. and Kimura, H. 2004. Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 18, 1165–1167.CrossRefPubMedGoogle Scholar
  24. Linden, D.R. 2014. Hydrogen sulfide signaling in the gastrointestinal tract. Antioxid. Redox Signal. 20, 818–830.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lisjak, M., Teklic, T., Wilson, I.D., Whiteman, M., and Hancock, J.T. 2013. Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ. 36, 1607–1616.CrossRefPubMedGoogle Scholar
  26. Mironov, A., Seregina, T., Nagornykh, M., Luhachack, L.G., Korolkova, N., Lopes, L.E., Kotova, V., Zavilgelsky, G., Shakulov, R., Shatalin, K., et al. 2017. Mechanism of H2S-mediated protection against oxidative stress in Escherichia coli. Proc. Natl. Acad. Sci. USA 114, 6022–6027.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mustafa, A.K., Gadalla, M.M., Sen, N., Kim, S., Mu, W., Gazi, S.K., Barrow, R.K., Yang, G., Wang, R., and Snyder, S.H. 2009. H2S signals through protein S-sulfhydration. Sci. Signal 2, ra72.PubMedPubMedCentralGoogle Scholar
  28. Olas, B. 2015. Hydrogen sulfide in signaling pathways. Clin. Chim. Acta 439, 212–218.CrossRefPubMedGoogle Scholar
  29. Ooi, X.J. and Tan, K.S. 2016. GSH mediates resistance to H2S toxicity in oral streptococci. Appl. Environ. Microbiol. 82, 2078–2085.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pietri, R., Román-Morales, E., and López-Garriga, J. 2011. Hydrogen sulfide and hemeproteins: knowledge and mysteries. Antioxid. Redox Signal. 15, 393–404.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pomposiello, P.J. and Demple, B. 2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol. 19, 109–114.CrossRefPubMedGoogle Scholar
  32. Renga, B. 2011. Hydrogen sulfide generation in mammals: the molecular biology of cystathionine-β-synthase (CBS) and cystathionine-γ-lyase (CSE). Inflamm. Allergy Drug Targets 10, 85–91.CrossRefPubMedGoogle Scholar
  33. Schairer, D.O., Chouake, J.S., Nosanchuk, J.D., and Friedman, A.J. 2012. The potential of nitric oxide releasing therapies as antimicrobial agents. Virulence 3, 271–279.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Semchyshyn, H., Bagnyukova, T., Storey, K., and Lushchak, V. 2005. Hydrogen peroxide increases the activities of soxRS regulon enzymes and the levels of oxidized proteins and lipids in Escherichia coli. Cell Biol. Int. 29, 898–902.CrossRefPubMedGoogle Scholar
  35. Shatalin, K., Shatalina, E., Mironov, A., and Nudler, E. 2011. H2S: a universal defense against antibiotics in bacteria. Science 334, 986–990.CrossRefPubMedGoogle Scholar
  36. Shibuya, N., Tanaka, M., Yoshida, M., Ogasawara, Y., Togawa, T., Ishii, K., and Kimura, H. 2009. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal. 11, 703–714.CrossRefGoogle Scholar
  37. Tanaka, A., Mulleriyawa, R.P., and Yasu, T. 1968. Possibility of hydrogen sulfide induced iron toxicity of the rice plant. Soil Sci. Plant Nutr. 14, 1–6.CrossRefGoogle Scholar
  38. Tapley, D.W., Buettner G.R., and Shick J.M. 1999. Free radicals and chemiluminescence as products of the spontaneous oxidation of sulfide in seawater, and their biological implications. Biol. Bull. 196, 52–56.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Vasil'eva, S.V., Stupakova, M.V., Lobysheva, I.I., Mikoyan, V.D., and Vanin, A.F. 2001. Activation of the Escherichia coli SoxRS-regulon by nitric oxide and its physiological donors. Biochem. (Mosc) 66, 984–988.CrossRefGoogle Scholar
  40. Wu, G., Wan, F., Fu, H., Li, N., and Gao, H. 2015. A matter of timing: contrasting effects of hydrogen sulfide on oxidative stress response in Shewanella oneidensis. J. Bacteriol. 197, 3563–3572.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Yakes, F.M. and Van Houten, B. 1997. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA 94, 514–519.CrossRefPubMedGoogle Scholar
  42. Zhang, H., Hu, L.Y., Hu, K.D., He, Y.D., Wang, S.H., and Luo, J.P. 2008. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J. Integr. Plant Biol. 50, 1518–1529.CrossRefPubMedGoogle Scholar
  43. Zhang, H., Jiao, H., Jiang, C.X., Wang, S.H., Wei, Z.J., Luo, J.P., and Jones, R.L. 2010. Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol. Plant. 32, 849–857.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  • Liu-Hui Fu
    • 1
  • Zeng-Zheng Wei
    • 1
  • Kang-Di Hu
    • 1
  • Lan-Ying Hu
    • 1
  • Yan-Hong Li
    • 1
  • Xiao-Yan Chen
    • 1
  • Zhuo Han
    • 1
  • Gai-Fang Yao
    • 1
  • Hua Zhang
    • 1
  1. 1.School of Food Science and EngineeringHefei University of TechnologyHefeiP. R. China

Personalised recommendations