1887

Abstract

Solar disinfection (SODIS) is used as an effective and inexpensive tool to improve the microbiological quality of drinking water in developing countries where no other means are available. Solar UVA light is the agent that inactivates bacteria during the treatment. Damage to bacterial membranes plays a crucial role in the inactivation process. This study showed that even slightly irradiated cells (after less than 1 h of simulated sunlight) were strongly affected in their ability to maintain essential parts of their energy metabolism, in particular of the respiratory chain (activities of NADH oxidase, succinate oxidase and lactate oxidase were measured). The cells' potential to generate ATP was also strongly inhibited. Many essential enzymes of carbon metabolism (glucose-6-phosphate dehydrogenase, glyceraldehyde-3-phosphate dehydrogenase, lactate dehydrogenase and malate dehydrogenase) and defence against oxidative stress (catalases and glutathione-disulfide reductase) were reduced in their activity during SODIS. The work suggests that damage to membrane enzymes is a likely cause of membrane dysfunction (loss of membrane potential and increased membrane permeability) during UVA irradiation. In this study, the first targets on the way to cell death were found to be the respiratory chain and FF ATPase.

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2010-07-01
2024-04-24
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References

  1. Allison W. S., Kaplan N. O. 1964; The comparative enzymology of triosephosphate dehydrogenase. J Biol Chem 239:2140–2152
    [Google Scholar]
  2. Anderson J. W., Foyer C. H., Walker D. A. 1983; Light-dependent reduction of dehydroascorbate and uptake of exogenous ascorbate by spinach chloroplasts. Planta 158:442–450
    [Google Scholar]
  3. Ascenzi J. M., Jagger J. 1979; Ultraviolet action spectrum (238–405 nm) for inhibition of glycine uptake in E. coli. Photochem Photobiol 30:661–666
    [Google Scholar]
  4. Berney M., Weilenmann H.-U., Egli T. 2006a; Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS. Microbiology 152:1719–1729
    [Google Scholar]
  5. Berney M., Weilenmann H. U., Simonetti A., Egli T. 2006b; Efficacy of solar disinfection of Escherichia coli, Shigella flexneri, Salmonella Typhimurium and Vibrio cholerae. J Appl Microbiol 101:828–836
    [Google Scholar]
  6. Bochner B. R. 2009; Global phenotypic characterization of bacteria. FEMS Microbiol Rev 33:191–205
    [Google Scholar]
  7. Bosshard F., Berney M., Scheifele M., Weilenmann H.-U., Egli T. 2009; Solar disinfection (SODIS) and subsequent dark storage of Salmonella typhimurium and Shigella flexneri monitored by flow cytometry. Microbiology 155:1310–1317
    [Google Scholar]
  8. Bosshard F., Riedel K., Schneider T., Geiser C., Bucheli M., Egli T. 2010; Protein oxidation and aggregation in UVA-irradiated Escherichia coli cells as signs of accelerated cellular senescence. Environ Microbiol (in press) [View Article]
    [Google Scholar]
  9. Bourdon E., Blache D. 2001; The importance of proteins in defence against oxidation. Antioxid Redox Signal 3:293–311
    [Google Scholar]
  10. 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
    [Google Scholar]
  11. Cabiscol E., Tamarit J., Ros J. 2000; Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
    [Google Scholar]
  12. Chamberlain J., Moss S. H. 1987; Lipid peroxidation and other membrane damage produced in Escherichia coli K1060 by near-UV radiation and deuterium oxide. Photochem Photobiol 45:625–630
    [Google Scholar]
  13. Choksi K. B., Nuss J. E., DeFord J. H., Papaconstantinou J. 2008; Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes. Free Radic Biol Med 45:826–838
    [Google Scholar]
  14. Claiborne A., Fridovich I. 1979; Purification of the o-dianisidine peroxidase from Escherichia coli B. Physicochemical characterization and analysis of its dual catalatic and peroxidatic activities. J Biol Chem 254:4245–4252
    [Google Scholar]
  15. Claiborne A., Malinowski D. P., Fridovich I. 1979; Purification and characterization of hydroperoxidase II of Escherichia coli B. J Biol Chem 254:11664–11668
    [Google Scholar]
  16. Conroy R. M., Meegan M. E., Joyce T., McGuigan K., Barnes J. 2001; Solar disinfection of drinking water protects against cholera in children under 6 years of age. Arch Dis Child 85:293–295
    [Google Scholar]
  17. D'Alessandro M., Turina P., Melandri B. A. 2008; Intrinsic uncoupling in the ATP synthase of Escherichia coli. Biochim Biophys Acta 17771518–1527
    [Google Scholar]
  18. Gianazza E., Crawford J., Miller I. 2007; Detecting oxidative post-translational modifications in proteins. Amino Acids 33:51–56
    [Google Scholar]
  19. Gonzalez-Flecha B., Demple B. 1995; Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270:13681–13687
    [Google Scholar]
  20. Hammes F., Berney M., Wang Y., Vital M., Koster O., Egli T. 2008; Flow-cytometric total bacterial cell counts as a descriptive microbiological parameter for drinking water treatment processes. Water Res 42:269–277
    [Google Scholar]
  21. Harm W. 1980 Biological Effects of Ultraviolet Radiation Cambridge: Cambridge University Press;
  22. Hoerter J. D., Arnold A. A., Kuczynska D. A., Shibuya A., Ward C. S., Sauer M. G., Gizachew A., Hotchkiss T. M., Fleming T. J., Johnson S. 2005; Effects of sublethal UVA irradiation on activity levels of oxidative defence enzymes and protein oxidation in Escherichia coli. J Photochem Photobiol B 81:171–180
    [Google Scholar]
  23. Imlay J. A. 2009; Oxidative stress, Module 5.4.4. In EcoSal Edited by Foster J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  24. Jiang Y., Rabbi M., Kim M., Ke C., Lee W., Clark R. L., Mieczkowski P. A., Marszalek P. E. 2009; UVA generates pyrimidine dimers in DNA directly. Biophys J 96:1151–1158
    [Google Scholar]
  25. John R. A. 2002; Photometric assays. In Enzyme Assays pp 49–78 Edited by Eisenthal R., Danson M. J. Oxford: Oxford University Press;
    [Google Scholar]
  26. Kohanski M. A., Dwyer D. J., Hayete B., Lawrence C. A., Collins J. J. 2007; A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810
    [Google Scholar]
  27. Komanapalli I. R., Mudd J. B., Lau B. H. S. 1997; Effect of ozone on metabolic activities of Escherichia coli K-12. Toxicol Lett 90:61–66
    [Google Scholar]
  28. Kunert K. J., Cresswell C. F., Schmidt A., Mullineaux P. M., Foyer C. H. 1990; Variations in the activity of glutathione reductase and the cellular glutathione content in relation to sensitivity to methylviologen in Escherichia coli. Arch Biochem Biophys 282:233–238
    [Google Scholar]
  29. Latch D. E., McNeill K. 2006; Microheterogeneity of singlet oxygen distributions in irradiated humic acid solutions. Science 311:1743–1747
    [Google Scholar]
  30. Levine R. L. 2002; Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic Biol Med 32:790–796
    [Google Scholar]
  31. Moss S. H., Smith K. C. 1981; Membrane damage can be a significant factor in the inactivation of Escherichia coli by near-ultraviolet radiation. Photochem Photobiol 33:203–210
    [Google Scholar]
  32. Murphey W. H., Barrie Kitto G., John M. L. 1969; Malate dehydrogenase from Escherichia coli. Methods Enzymol 13:145–147
    [Google Scholar]
  33. Nicholls D. G., Ferguson S. 1992 Bioenergetics 3 London: Academic Press;
  34. Niki E., Yoshida Y., Saito Y., Noguchi N. 2005; Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun 338:668–676
    [Google Scholar]
  35. Robb F. T., Hauman J. H., Peak M. J. 1978; Similar spectra for the inactivation by monochromatic light of two distinct leucine transport systems in Escherichia coli. Photochem Photobiol 27:465–469
    [Google Scholar]
  36. Sharma R. C., Jagger J. 1981; Ultraviolet (254–405 nm) action spectrum and kinetic studies of alanine uptake in Escherichia coli B/R. Photochem Photobiol 33:173–177
    [Google Scholar]
  37. Switala J., Loewen P. C. 2002; Diversity of properties among catalases. Arch Biochem Biophys 401:145–154
    [Google Scholar]
  38. Tarmy E. M., Kaplan N. O. 1968; Chemical characterization of d-lactate dehydrogenase from Escherichia coli B. J Biol Chem 243:2579–2586
    [Google Scholar]
  39. Unden G., Dünnwald P. 2008; The aerobic and anaerobic respiratory chain of Escherichia coli and Salmonella enterica: enzymes and energetics, Module 3.2.2. In EcoSal Edited by Stewart V. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  40. Visick J. E., Clarke S. 1997; RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol 179:4158–4163
    [Google Scholar]
  41. Voss P., Hajimiragha H., Engels M., Ruhwiedel C., Calles C., Schroeder P., Grune T. 2007; Irradiation of GAPDH: a model for environmentally induced protein damage. Biol Chem 388:583–592
    [Google Scholar]
  42. Wang Y., Hammes F., Boon N., Egli T. 2007; Quantification of the filterability of freshwater bacteria through 0.45, 0.22, and 0.1 μm pore size filters and shape-dependent enrichment of filterable bacterial communities. Environ Sci Technol 41:7080–7086
    [Google Scholar]
  43. Wegelin M., Canonica S., Mechsner K., Fleischmann T., Pesaro F., Metzler A. 1994; Solar water disinfection: scope of the process and analysis of radiation experiments. Aqua 43:154–169
    [Google Scholar]
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