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Wavelength dependence of biological damage induced by UV radiation on bacteria

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Abstract

The biological effects of UV radiation of different wavelengths (UVA, UVB and UVC) were assessed in nine bacterial isolates displaying different UV sensitivities. Biological effects (survival and activity) and molecular markers of oxidative stress [DNA strand breakage (DSB), generation of reactive oxygen species (ROS), oxidative damage to proteins and lipids, and the activity of antioxidant enzymes catalase and superoxide dismutase] were quantified and statistically analyzed in order to identify the major determinants of cell inactivation under the different spectral regions. Survival and activity followed a clear wavelength dependence, being highest under UVA and lowest under UVC. The generation of ROS, as well as protein and lipid oxidation, followed the same pattern. DNA damage (DSB) showed the inverse trend. Multiple stepwise regression analysis revealed that survival under UVA, UVB and UVC wavelengths was best explained by DSB, oxidative damage to lipids, and intracellular ROS levels, respectively.

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References

  • Abboudi M, Surget SM, Rontani JF, Sempéré R, Joux F (2008) Physiological alteration of the marine bacterium Vibrio angustum S14 exposed to simulated sunlight during growth. Curr Microbiol 57:412–417

    Article  PubMed  CAS  Google Scholar 

  • Alonso-Sáez L, Gasol JM, Lefort T, Hofer J, Sommaruga R (2006) Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in Northwestern Mediterranean coastal waters. Appl Environ Microbiol 72:5806–5813

    Article  PubMed  Google Scholar 

  • Anderl JN, Zahller J, Roe F, Stewart PS (2003) Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 47:1251–1256

    Article  PubMed  CAS  Google Scholar 

  • Arrieta JM, Weinbauer MG, Herndl GJ (2000) Interspecific variability in sensitivity to UV radiation and subsequent recovery in selected isolates of marine bacteria. Appl Environ Microbiol 66:1468–1473

    Article  PubMed  CAS  Google Scholar 

  • Bauermeister A, Bentchikou E, Moeller R, Rettberg P (2009) Roles of PprA, IrrE, and RecA in the resistance of Deinococcus radiodurans to germicidal and environmentally relevant UV radiation. Arch Microbiol 191:913–918

    Article  PubMed  CAS  Google Scholar 

  • Beers RFJ, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    PubMed  CAS  Google Scholar 

  • Berney M, Weilenmann H-U, Egli T (2006a) Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environ Microbiol 8:1635–1647

    Article  PubMed  CAS  Google Scholar 

  • Berney M, Weilenmann HU, Ihssen J, Bassin C, Egli T (2006b) Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Appl Environ Microbiol 72:2586–2593

    Article  PubMed  CAS  Google Scholar 

  • Berney M, Weilenmann HU, Simonetti A, Egli T (2006c) Efficacy of solar disinfection of Escherichia coli, Shigella flexneri, Salmonella typhimurium and Vibrio cholerae. J Appl Microbiol 101:828–836

    Article  PubMed  CAS  Google Scholar 

  • Bosshard F, Bucheli M, Meur Y, Egli T (2010a) The respiratory chain is the cell’s Achilles’ heel during UVA inactivation in Escherichia coli. Microbiology 156:2006–2015

    Article  PubMed  CAS  Google Scholar 

  • Bosshard F, Riedel K, Schneider T, Geiser C, Bucheli M, Egli T (2010b) Protein oxidation and aggregation in UVA-irradiated Escherichia coli cells as signs of accelerated cellular senescence. Environ Microbiol 12:2931–2945

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (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

    Article  PubMed  CAS  Google Scholar 

  • Cadet J, Courdavault S, Ravanat JL, Douki T (2005) UVB and UVA radiation-mediated damage to isolated and cellular DNA. Pure Appl Chem 77:947–961

    Article  CAS  Google Scholar 

  • Chamberlain J, Moss SH (1987) Lipid peroxidation and other membrane damage produced in Escherichia coli K1060 by near-UV radiation and deuterium oxide. Photochem Photobiol 45:625–630

    Article  PubMed  CAS  Google Scholar 

  • Chun H, Kim J, Chung K, Won M, Song KB (2009) Inactivation kinetics of Listeria monocytogenes, Salmonella enterica serovar Typhimurium, and Campylobacter jejuni in ready-to-eat sliced ham using UV-C irradiation. Meat Sci 83:599–603

    Article  PubMed  CAS  Google Scholar 

  • Coohill TP, Sagripanti J-L (2008) Overview of the inactivation by 254 nm ultraviolet radiation of bacteria with particular relevance to biodefense. Photochem Photobiol 84:1084–1090

    PubMed  CAS  Google Scholar 

  • Coohill TP, Sagripanti J-L (2009) Bacterial inactivation by solar ultraviolet radiation compared with sensitivity to 254 nm radiation. Photochem Photobiol 85:1043–1052

    Article  PubMed  CAS  Google Scholar 

  • De La Vega UP, Rettberg P, Douki T, Cadet J, Horneck G (2005) Sensitivity to polychromatic UV-radiation of strains of Deinococcus radiodurans differing in their DNA repair capacity. Int J Radiat Biol 81:601–611

    Article  Google Scholar 

  • Di Capua C, Bortolotti A, Farías ME, Cortez N (2011) UV-resistant Acinetobacter sp. isolates from Andean wetlands display high catalase activity. FEMS Microbiol Lett 317:181–189

    Article  PubMed  Google Scholar 

  • Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch Microbiol 177:322–331

    Article  PubMed  CAS  Google Scholar 

  • Dodson ML, Michaels ML, Lloyd RS (1994) Unified catalytic mechanism for DNA glycosylases. J Biol Chem 269:32709–32712

    PubMed  CAS  Google Scholar 

  • Eisenstark A (1998) Bacterial gene products in response to near-ultraviolet radiation. Mutat Res Fund Mol M 422:85–95

    Article  CAS  Google Scholar 

  • Fernández Zenoff V, Siñeriz F, Farías ME (2006) Diverse responses to UV-B radiation and repair mechanisms of bacteria isolated from high-altitude aquatic environments. Appl Environ Microbiol 72:7857–7863

    Article  PubMed  Google Scholar 

  • Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. American Society of Microbiology Press, Washington, DC

    Google Scholar 

  • Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717

    Article  Google Scholar 

  • Girotti AW (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res 39:1529–1542

    PubMed  CAS  Google Scholar 

  • Gomes AA et al (2005) Reactive oxygen species mediate lethality induced by far-UV in Escherichia coli cells. Redox Rep 10:91–95

    Article  PubMed  CAS  Google Scholar 

  • He YY, Häder DP (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol, B 66:115–124

    Article  CAS  Google Scholar 

  • Hernandez EA, Ferreyra GA, Mac Cormack WP (2006) Response of two Antarctic marine bacteria to different natural UV radiation doses and wavelengths. Antarct Sci 18:205–212

    Article  Google Scholar 

  • Hobbie JE, Daley RJ, Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed  CAS  Google Scholar 

  • Hörtnagl P, Pérez MT, Sommaruga R (2011) Contrasting effects of ultraviolet radiation on the growth efficiency of freshwater bacteria. Aquat Ecol 45:125–136

    Article  PubMed  Google Scholar 

  • Ikehata H et al (2008) UVA1 genotoxicity is mediated not by oxidative damage but by cyclobutane pyrimidine dimers in normal mouse skin. J Invest Dermatol 128:2289–2296

    Article  PubMed  CAS  Google Scholar 

  • Imlay JA (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59:1073–1082

    Article  PubMed  Google Scholar 

  • Jacobs JL, Sundin GW (2001) Effect of solar UV-B radiation on a phyllosphere bacterial community. Appl Environ Microbiol 67:5488–5496

    Article  PubMed  CAS  Google Scholar 

  • Jagger J (1985) Solar UV actions on living cells. Praeger Publishing, New York

    Google Scholar 

  • Joux F, Jeffrey WH, Lebaron P, Mitchell DL (1999) Marine bacterial isolates display diverse responses to UV-B radiation. Appl Environ Microbiol 65:3820–3827

    PubMed  CAS  Google Scholar 

  • King B, Kesavan J, Sagripanti J-L (2011) Germicidal UV sensitivity of bacteria in aerosols and on contaminated surfaces. Aerosol Sci Tech 45:645–653

    Article  CAS  Google Scholar 

  • Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci USA 107:14373–14377

    Article  PubMed  CAS  Google Scholar 

  • Matallana-Surget S, Meador JA, Joux F, Douki T (2008) Effect of the GC content of DNA on the distribution of UVB-induced bipyrimidine photoproducts. Photoch Photobio Sci 7:794–801

    Article  CAS  Google Scholar 

  • Matallana-Surget S, Joux F, Raftery MJ, Cavicchioli R (2009a) The response of the marine bacterium Sphingopyxis alaskensis to solar radiation assessed by quantitative proteomics. Environ Microbiol 11:2660–2675

    Article  PubMed  CAS  Google Scholar 

  • Matallana-Surget SM, Douki T, Cavicchioli R, Joux F (2009b) Remarkable resistance to UVB of the marine bacterium Photobacterium angustum explained by an unexpected role of photolyase. Photoch Photobio Sci 8:1313–1320

    Article  CAS  Google Scholar 

  • Matallana-Surget S, Joux F, Wattiez R, Lebaron P (2012) Proteome analysis of the UVB-resistant marine bacterium Photobacterium angustum S14. PLoS ONE 7:e42299

    Article  PubMed  CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    PubMed  CAS  Google Scholar 

  • Misiaszek R, Crean C, Joffe A, Geacintov NE, Shafirovich V (2004) Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J Biol Chem 279:32106–32115

    Article  PubMed  CAS  Google Scholar 

  • Mitchell DL, Karentz D (1993) The induction and repair of DNA photodamage in the environment. In: Young AR, Bjorn LO, Moan J, Nultsch W (eds) Environmental UV photobiology. Plenum Press, New York, pp 345–377

  • Moan J, Peak MJ (1989) Effects of UV radiation on cells. J Photochem Photobiol, B 4:21–34

    Article  CAS  Google Scholar 

  • Moeller R et al (2010) Genomic bipyrimidine nucleotide frequency and microbial reactions to germicidal UV radiation. Arch Microbiol 192:521–529

    Article  PubMed  CAS  Google Scholar 

  • Murphy TM, Huerta AJ (1990) Hydrogen peroxide formation in cultured rose cells in response to UV-C radiation. Physiol Plantarum 78:247–253

    Article  CAS  Google Scholar 

  • Ordoñez O, Flores M, Dib J, Paz A, Farías M (2009) Extremophile culture collection from Andean Lakes: extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microb Ecol 58:461–473

    Article  PubMed  Google Scholar 

  • Pattison DI, Davies MJ (2006) Actions of ultraviolet light on cellular structures. EXS 96:131-157

    Google Scholar 

  • Pérez JM et al. (2007) Bacterial toxicity of potassium tellurite: Unveiling an ancient enigma. PLoS ONE 2:e211

    Google Scholar 

  • Pfeifer GP (1997) Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochem Photobiol 65:270–283

    Article  PubMed  CAS  Google Scholar 

  • Pizarro RA, Orce LV (1988) Membrane damage and recovery associated with growth delay induced by near-UV radiation in Escherichia coli K-12. Photochem Photobiol 47:391–397

    Article  PubMed  CAS  Google Scholar 

  • Qiu X, Sundin GW, Chai B, Tiedje JM (2004) Survival of Shewanella oneidensis MR-1 after UV radiation exposure. Appl Environ Microbiol 70:6435–6443

    Article  PubMed  CAS  Google Scholar 

  • Qiu X, Sundin GW, Wu L, Zhou J, Tiedje JM (2005) Comparative analysis of differentially expressed genes in Shewanella oneidensis MR-1 following exposure to UVC, UVB, and UVA radiation. J Bacteriol 187:3556–3564

    Article  PubMed  CAS  Google Scholar 

  • Rünger TM, Farahvash B, Hatvani Z, Rees A (2012) Comparison of DNA damage responses following equimutagenic doses of UVA and UVB: a less effective cell cycle arrest with UVA may render UVA-induced pyrimidine dimers more mutagenic than UVB-induced ones. Photoch Photobio Sci 11:207–215

    Article  Google Scholar 

  • Santos AL et al (2011) Diversity in UV sensitivity and recovery potential among bacterioneuston and bacterioplankton isolates. Lett Appl Microbiol 52:360–366

    Article  PubMed  CAS  Google Scholar 

  • Santos AL et al (2012a) The UV responses of bacterioneuston and bacterioplankton isolates depend on the physiological condition and involve a metabolic shift. FEMS Microbiol Ecol 80:646–658

    Article  PubMed  CAS  Google Scholar 

  • Santos AL et al (2012b) Effects of UV-B radiation on the structural and physiological diversity of bacterioneuston and bacterioplankton. Appl Environ Microbiol 78:2066–2069

    Article  PubMed  CAS  Google Scholar 

  • Schenk M, Raffellini S, Guerrero S, Blanco GA, Alzamora SM (2011) Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae by UV-C light: study of cell injury by flow cytometry. LWT Food Sci Technol 44:191–198

    Article  CAS  Google Scholar 

  • Semchyshyn H, Bagnyukova T, Storey K, 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

    Article  PubMed  CAS  Google Scholar 

  • Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262

    Article  PubMed  CAS  Google Scholar 

  • Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using tritiated-leucine. Mar Microb Food Webs 6:107–114

    Google Scholar 

  • Sundin GW, Jacobs JL (1999) Ultraviolet radiation (UVR) sensitivity analysis and UVR survival strategies of a bacterial community from the phyllosphere of field-grown peanut (Arachis hypogeae L.). Microb Ecol 38:27–38

    Article  PubMed  Google Scholar 

  • Ubomba-Jaswa E, Navntoft C, Polo-López MI, Fernandez-Ibáñez P, McGuigan KG (2009) Solar disinfection of drinking water (SODIS): an investigation of the effect of UV-A dose on inactivation efficiency. Photoch Photobio Sci 8:587–595

    Article  CAS  Google Scholar 

  • Visser PM, Poos JJ, Scheper BB, Boelen P, Van Duyl FC (2002) Diurnal variations in depth profiles of UV-induced DNA damage and inhibition of bacterioplankton production in tropical coastal waters. Mar Ecol Prog Ser 228:25–33

    Article  CAS  Google Scholar 

  • Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J (2005) Abundances, identity, and growth state of Actinobacteria in mountain lakes of different UV transparency. Appl Environ Microbiol 71:5551–5559

    Article  PubMed  CAS  Google Scholar 

  • Zeeshan M, Prasad SM (2009) Differential response of growth, photosynthesis, antioxidant enzymes and lipid peroxidation to UV-B radiation in three cyanobacteria. S Afr J Bot 75:466–474

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank the anonymous reviewers and editors who provided helpful criticism and suggestions which greatly contributed to improve the original manuscript. Acknowledgments are due to Francisco Coelho and Abel Ferreira for assistance in UV intensity measurements and to Prof. Rosário Correia (Physics Department, Universiy of Aveiro) for reviewing the manuscript. Financial support for this work was provided by CESAM (Centre for Environmental and Marine Studies, University of Aveiro) and the Portuguese Foundation for Science and Technology (FCT) in the form of a PhD grant to A. L. Santos (SFRH/BD/40160/2007) and a post-Doctoral grant to I. Henriques (SFRH/BPD/63487/2009).

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  1. Department of Biology & CESAM, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Ana L. Santos, Vanessa Oliveira, Inês Baptista, Isabel Henriques, Newton C. M. Gomes, Adelaide Almeida, António Correia & Ângela Cunha

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  1. Ana L. Santos
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  2. Vanessa Oliveira
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  3. Inês Baptista
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Correspondence to Ângela Cunha.

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Communicated by Erko Stackebrandt.

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Santos, A.L., Oliveira, V., Baptista, I. et al. Wavelength dependence of biological damage induced by UV radiation on bacteria. Arch Microbiol 195, 63–74 (2013). https://doi.org/10.1007/s00203-012-0847-5

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  • DOI: https://doi.org/10.1007/s00203-012-0847-5

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