Skip to main content
Log in

Comparing TiO2 photocatalysis and UV-C radiation for inactivation and mutant formation of Salmonella typhimurium TA102

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Salmonellosis is one of the most common causes of foodborne bacterial human disease worldwide, and the emergence of multidrug-resistant (MDR) strains of Salmonella enterica serovar Typhimurium (S. typhimurium) was associated to the incidence of invasive salmonellosis. The objective of the present work was to investigate the effects of the TiO2 photocatalysis process in terms of both bacteria inactivation and the emergence of mutants, on S. typhimurium TA102 water suspensions. The TiO2 photocatalysis was compared with a conventional disinfection process such as UV-C radiation. In spite of the faster bacterial inactivation obtained in UV-C disinfection experiments (45, 15, and 10 min for total inactivation for initial cell density 109, 108, and 107 CFU mL−1, respectively), photocatalytic disinfection (60, 30, and 15 min) was more energy efficient because of a lower energy requirement (2–20 mWs cm−2) compared to the UV-C disinfection process (5–30 mWs cm−2). During the photocatalytic experiments, the mutation frequency increased up to 1648-fold compared to background level for a 108 CFU mL−1 initial bacterial density, and mutants were inactivated after 1–10-min treatment, depending on initial bacterial cell density. In UV-C disinfection experiments, the mutation frequency increased up to 2181-fold for a 108 CFU mL−1 initial bacterial cell density, and UV-C doses in the range of 0.5–4.8 mWs cm−2 were necessary to decrease mutation frequency. In conclusion, both disinfection processes were effective in the inactivation of S. typhimurium cells, and mutants released into the environment can be avoided if cells are effectively inactivated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Berney HU, Weilenmann A, Simonetti T (2006) Efficacy of solar disinfection of Escherichia coli, Shigella flexneri, Salmonella typhimurium and Vibrio cholerae. J Appl Microbiol 101(4):828–836

    Article  CAS  Google Scholar 

  • Cho M, Chung H, Choi W, Yoon J (2004) Linear correlation between inactivation of E. coli and OH radical concentration in TiO2 photocatalytic disinfection. Water Res 38:1069–1077

    Article  CAS  Google Scholar 

  • Dalrymple OK, Stefanakos E, Trotz MA, Goswami DY (2010) A review of the mechanisms and modeling of photocatalytic disinfection. Appl Catalysis B: Environ 98:27–38

    Article  CAS  Google Scholar 

  • de Kok TM, van Maanen JM, Lankelma J, ten Hoor F, Kleinjans JC (1992) Electron spin resonance spectroscopy of oxygen radicals generated by synthetic fecapentaene-12 and reduction of fecapentaene mutagenicity to Salmonella typhimurium by hydroxyl radical scavenging. Carcinogenesis 13:1249–1255

    Article  Google Scholar 

  • Dunlop PSM, Ciavola M, Rizzo L, Byrne JA (2011) Inactivation and injury assessment of Escherichia coli during solar and photocatalytic disinfection in LDPE bags. Chemosphere 85:1160–1166

    Article  CAS  Google Scholar 

  • Fàbrega A, Vila J (2013) Salmonella enterica serovar typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26(2):308–341

    Article  Google Scholar 

  • Foster HA, Ditta IB, Varghese S, Steele A (2011) Photocatalytic disinfection using titanium dioxide: spectrum and mechanism of antimicrobial activity. Appl Microbiol Biotechnol 90(6):1847–1868

    Article  CAS  Google Scholar 

  • Gordon MA, Graham SM, Walsh AL, Wilson LK, Phiri A, Molyneux EM et al (2008) Epidemics of invasive Salmonella enterica serovar enteritidis and Salmonella enterica serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46:963–969

    Article  Google Scholar 

  • Grey CE, Adlercreutz P (2003) Ability of antioxidants to prevent oxidative mutations in Salmonella typhimurium TA102. Mutat Res 527:27–36

    Article  CAS  Google Scholar 

  • Grossweiner LI, Jones LR, Grossweiner JB, Rogers BHG (2005) Photochemical damage to biological systems. In The Science of Phototherapy: an Introduction (Ed Jones), Springer the Netherlands.

  • Haley BJ, Cole D (2009) Distribution, diversity, and seasonality of waterborne salmonellae in a rural watershed. Appl Environ Microb 75(5):1248–1255

    Article  CAS  Google Scholar 

  • Hignen WAM, Medema GJ (2006) Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res 40(1):3–22

    Article  Google Scholar 

  • Kanno T, Nakamura K, Ikai H, Kikuchi K, Sasaki K, Niwano Y (2012) Literature review of the role of hydroxyl radicals in chemicallyinduced mutagenicity and carcinogenicity for the risk assessment of a disinfection system utilizing photolysis of hydrogen peroxide. J Clin Biochem Nutr 51:9–14

    Article  CAS  Google Scholar 

  • Koivunen J, Heinonen-Tanski H (2005) Inactivation of enteric microorganisms with chemical disinfectants, UV radiation and combined chemical/UV treatments. Water Res 39(8):1519–1526

    Article  CAS  Google Scholar 

  • Levantesi C, La Mantia R, Masciopinto C, Uta Böckelmann C et al (2010) Quantification of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. Sci Total Environ 408(21):4923–4230

    Article  CAS  Google Scholar 

  • Levantesi C, Bonadonna L, Briancesco R, Grohmann E, Toze S, Tandoi V (2012) Salmonella in surface and drinking water: occurrence and water-mediated transmission. Food Res Int 45(2):587–602

    Article  Google Scholar 

  • Li H, Bhaskara A, Megalis C, Tortorello ML (2012) Transcriptomic analysis of Salmonella desiccation resistance. Foodborne Pathog Dis 9:1143–1151

    Article  CAS  Google Scholar 

  • Long M, Wang J, Zhuang H, Zhang Y, Wu H, Zhang J (2014) Performance and mechanism of standard nano-TiO2 (P-25) in photocatalytic disinfection of foodborne microorganisms—Salmonella typhimurium and Listeria monocytogenes. Food Control 39(1):68–74

    Article  CAS  Google Scholar 

  • Lu Z-X, Zhou L, Zhang Z-L, Shi W-L, Xie Z-X, Xie H-Y, Pang D-W, Shen P (2003) Cell damage induced by photocatalysis of TiO2 thin films. Langmuir 19:8765–8768

    Article  CAS  Google Scholar 

  • Magdeburg A, Stalter D, Schlsener M, Ternes T, Oehlmann J (2014) Evaluating the efficiency of advanced wastewater treatment: target analysis of organic contaminants and (geno-)toxicity assessment tell a different story. Water Res 50(0):35–47

    Article  CAS  Google Scholar 

  • Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889

    Article  Google Scholar 

  • Maron DM, Ames BN (1983) Revised methods for Salmonella mutagenicity test. Mutat Res 101:173–215

    Article  Google Scholar 

  • Martinez-Urtaza J, Saco M, de Novoa J, Perez-Pineiro P, Peiteado J, Lozano-Leon A, Garcia-Martin O (2004) Influence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Appl Environ Microbiol 70:2089–2097

    Article  CAS  Google Scholar 

  • Masarikova M, Manga I, Cizek A, Dolejska M, Oravcova V, Myskova P, Karpiskova R, Literak I (2016) Salmonella enterica resistant to antimicrobials in wastewater effluents and black-headed gulls in the Czech Republic, 2012. Sci Total Environ 542:102–107

    Article  CAS  Google Scholar 

  • McGuigan KG, Conroy RM, Mosler H-J, du Preez M, Ubomba-Jaswa E, Fernandez-Ibanez P (2012) Solar water disinfection (SODIS): a review from bench-top to roof-top. J Hazard Mater 235(236):29–46

    Article  Google Scholar 

  • Michael GB, Butaye P, Cloeckaert A, Schwarz S (2006) Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microbes Infect 8(7):1898–1914

    Article  CAS  Google Scholar 

  • Mišík M, Knasmueller S, Ferk F, Cichna-Markl M, Grummt T, Schaar H, Kreuzinger N (2011) Impact of ozonation on the genotoxic activity of tertiary treated municipalwastewatr. Water Res 45(12):3681–3691

    Article  Google Scholar 

  • Monarca S, Feretti D, Collivignarelli C, Guzzella G, Zerbini I, Bertanza G, Pedrazzani R (2000) The influence of different disinfectants on mutagenicity and toxicity of urban wastewater. Water Res 34(17):4261–4269

    Article  CAS  Google Scholar 

  • Nutt JD, Li X, Woodward CL, Zabala-Diaz IB, Ricke SC (2003) Growth kinetics response of a Salmonella typhimurium poultry marker strain to fresh produce extracts. Bioresource Technol 89:313–316

    Article  CAS  Google Scholar 

  • Oubrim N, Ennaji MM, Badri S, Cohen N (2012) Removal of antibiotic-resistant Salmonella in sewage water from wastewater treatment plants in Settat and Soualem, Morocco. Eur J Sci Res 68(4):565–573

    Google Scholar 

  • Polo F, Figueras MJ, Inza I, Sala J, Fleisher JM, Guarro J (1999) Prevalence of Salmonella serotypes in environmental waters and their relationships with indicator organisms. A Van Leeuw 75:285–292

    Article  CAS  Google Scholar 

  • Polo-López MI, Castro-Alférez M, Oller I, Fernández-Ibáñez P (2014) Assessment of solar photo-Fenton, photocatalysis, and H2O2 for removal of phytopathogen fungi spores in synthetic and real effluents of urban wastewater. Chemi Eng J 257:122–130

    Article  Google Scholar 

  • Popoff MY (2001) Antigenic formulas of the salmonella serovars. In: WHO collaborating Center for Reference and Research on salmonella, 8th edn. Institut Pasteur Paris, France

    Google Scholar 

  • Rahman BA, Wasfy MO, Maksoud MA, Hanna N, Dueger E, House B (2014) Multi-drug resistance and reduced susceptibility to ciprofloxacin among Salmonella enterica serovar typhi isolates from the Middle East and Central Asia. New Microbes and New Infect 2(4):88–92

    Article  CAS  Google Scholar 

  • Rahmani M, Peighambari SM, Svendsen CA, Cavaco LM, Agersø Y, Hendriksen RS (2013) Molecular clonality and antimicrobial resistance in Salmonella enterica serovars enteritidis and Infantis from broilers in three northern regions of Iran. BMC Vet Res 9:66

    Article  Google Scholar 

  • Rincon AG, Pulgarin C (2007) Fe3+ and TiO2 solar-light-assisted inactivation of E. coli at field scale—implications in solar disinfection at low temperature of large quantities of water. Catal Today 122:128–136

    Article  CAS  Google Scholar 

  • Rizzo L (2011) Bioassays as a tool for evaluating advanced oxidation processes in water and wastewater treatment. Water Res 45:4311–4330

    Article  CAS  Google Scholar 

  • Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    Article  CAS  Google Scholar 

  • Rizzo L, Ferro G, Manaia CM (2014a) Wastewater disinfection by solar heterogeneous photocatalysis: effect on tetracycline resistant/sensitive enterococcus strains. Global Nest J 16:455–462

    Google Scholar 

  • Rizzo L, Della Sala A, Fiorentino A, Li Puma G (2014b) Disinfection of urban wastewater by solar driven and UV lamp-TiO2 photocatalysis: effect on a multi drug resistant Escherichia coli strain. Water Res 53:145–152

    Article  CAS  Google Scholar 

  • Robertson GP (2005) Functional and therapeutic significance of Akt deregulation in malignant melanoma. Cancer Metast Rev 24:273–285

    Article  CAS  Google Scholar 

  • Sciacca J, Rengifo-Herrera J, Wethe PC (2011) Solar disinfection of wild Salmonella sp. in natural water with a 18 L CPC photoreactor: detrimental effect of non-sterile storage of treated water. Sol Energy 85:1399–1408

    Article  CAS  Google Scholar 

  • Sharma VK, Johnson N, Cizmas L, McDonald TJ, Kim H (2016) A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere 150:702–714

    Article  CAS  Google Scholar 

  • Silva RC, Cardoso WM, Teixeira RSC, Albuquerque ÁH, Horn RV, Cavalcanti CM (2013) Salmonella Gallinarum virulence in experimentally infected Japanese quails (Coturnix japonica). Braz J of Poult Sci 15(1):39–45

    Google Scholar 

  • Simonet J, Gantzer C (2006) Inactivation of poliovirus 1 and F-specific RNA phages and degradation of their genomes by UV irradiation at 254 nanometers. Appl Environ Microbiol 72(12):7671–7677

    Article  CAS  Google Scholar 

  • Sinha RP, Häder DP (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1(4):225–236

    Article  CAS  Google Scholar 

  • Tate P, Stannera A, Shieldsa K, Smithc S, Larcom L (2006) Blackberry extracts inhibit UV-induced mutagenesis in Salmonella typhimurium TA100. Nutr Res 26:100–104

    Article  CAS  Google Scholar 

  • Wang J, Zhuan H, Hinton A Jr, Bowker B, Zhang J (2014) Photocatalytic disinfection of spoilage bacteria Pseudomonas fluorescens and Macrococcus caseolyticus by nano-TiO2. LWT Food Sci Technol 59(2):1009–1017

    Article  CAS  Google Scholar 

  • Wéry N, Lhoutellier C, Ducray F, Delgenès JP, Godon JJ (2008) Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Res 42:53–62

    Article  Google Scholar 

Download references

Acknowledgments

The support of University of Salerno through FARB2012 (Trattamento avanzato di acque reflue urbane mediante fotocatalisi: effetto sui batteri resistenti agli antibiotici) project funding is acknowledged. The authors would like also to acknowledge the financial support provided by COST-European Cooperation in Science and Technology, to the COST Action “TD0803: Detecting evolutionary hotspots of antibiotic resistances in Europe (DARE)” and COST Action “ES1403: New and emerging challenges and opportunities in wastewater reuse (NEREUS).” CM wishes to thank the “Zone Atelier Moselle” (ZAM) for supporting his research on treatment processes and their effects.

Disclaimer

The content of this article is the authors’ responsibility and neither COST nor any person acting on its behalf is responsible for the use, which might be made of the information contained in it.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luigi Rizzo.

Additional information

Responsible editor: Gerald Thouand

Electronic supplementary material

.

ESM 1

(DOCX 552 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fiorentino, A., Rizzo, L., Guilloteau, H. et al. Comparing TiO2 photocatalysis and UV-C radiation for inactivation and mutant formation of Salmonella typhimurium TA102. Environ Sci Pollut Res 24, 1871–1879 (2017). https://doi.org/10.1007/s11356-016-7981-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7981-6

Keywords

Navigation