Technical Papers
Apr 11, 2023

Tolerance Increase in Escherichia coli O157:H7 and Methicillin-Resistant Staphylococcus Aureus USA300 Exposed to Low-Power Continuous Ultraviolet Radiation from Narrow-Wavelength Sources

Publication: Journal of Environmental Engineering
Volume 149, Issue 6

Abstract

Escherichia coli O157:H7 is a major cause of foodborne disease outbreaks throughout the world, while methicillin-resistant Staphylococcus aureus (MRSA) is responsible for many difficult-to-treat infections in humans. Ultraviolet (UV) irradiation is commonly used for disinfection in food processing, medical facilities, and water treatment to prevent the transmission of these pathogen. With increased use of UV disinfection technologies over the last few years because of COVID-19 and concerns about other communicable disease, it has become a concern that microbial species could develop tolerance to UV irradiation, especially when it is applied continuously. To elucidate the effect of continuous UV exposure at different wavelengths and power levels on the tolerance development of bacteria, Escherichia coli O157:H7 and MRSA)USA300 growths were investigated by continuously exposing inoculated agar plates to six different commercially available UV sources at wavelengths of 222 nm, 254 nm, 275 nm, and 405 nm. The agar plates in these experiments were partially covered by a thin acrylic sheet, which provided either complete protection from the UV to the cells directly under the sheet, no protection if significantly away from the sheet, or partial protection near the edges of the sheet due to shading or small amounts of UV reflection under the sheet at the edges. In these experiments, tolerant cells of E. coli and S. aureus were found from the 222 nm, the 405 nm, and one of the 254 nm sources. Upon examination of the power of each UV source, it was shown that the 275 nm and 254 nm sources that resulted in no tolerant cells had surface power densities [at 25 cm (10 in.)] that were more than 10–200 times greater than those that had tolerant cells. These results suggests that bacterial cells have a higher chance to develop UV tolerance under lower power UV sources (under the experimental conditions in our laboratory). Genome investigation of the tolerant colonies revealed that there are no significant differences between the cells that developed tolerance and the original organism, hinting at the need to explore the role of epigenetics mechanisms in the development of UV tolerance in these bacteria.

Get full access to this article

View all available purchase options and get full access to this article.

Data Availability Statement

All data, models, or code that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

We thank Prof. N. Nitin, University of California, Davis, for providing the Escherichia coli O157:H7 samples to us. This research was funded in part by the Defense Logistics Agency Contract No. SP4701-19-C-0039, the National Oceanic and Atmospheric Administration Award ID NA21OAR0210304, and the Department of Energy Contract No. DE-SC0021692.

References

Aichi, M., N. Takatani, and T. Omata. 2001. “Role of NtcB in activation of nitrate assimilation genes in the cyanobacterium Synechocystis sp. strain PCC 6803.” J. Bacteriol. 183 (20): 5840–5847. https://doi.org/10.1128/JB.183.20.5840-5847.2001.
Boyce, J. M. 2016. “Modern technologies for improving cleaning and disinfection of environmental surfaces in hospitals.” Antimicrob. Resist. Infect. Control 5 (1): 1–10. https://doi.org/10.1186/s13756-016-0111-x.
Bustos, Y., M. Vaca, R. López, E. Bandala, L. Torres, and N. Rojas-Valencia. 2014. “Disinfection of primary municipal wastewater effluents using continuous UV and ozone treatment.” J. Water Resour. Prot. 6 (1): 16–21. https://doi.org/10.4236/jwarp.2014.61003.
Choi, H., P. Chatterjee, M. Hwang, E. M. Stock, J. S. Lukey, J. E. Zeber, and C. Jinadatha. 2022. “Can multidrug-resistant organisms become resistant to ultraviolet (UV) light following serial exposures? Characterization of post-UV genomic changes using whole-genome sequencing.” Infect. Control Hosp. Epidemiol. 43 (1): 72–78. https://doi.org/10.1017/ice.2021.51.
Day, T. 2016. “Interpreting phenotypic antibiotic tolerance and persister cells as evolution via epigenetic inheritance.” Mol. Ecol. 25 (8): 1869–1882. https://doi.org/10.1111/mec.13603.
Dib, J., J. Motok, V. F. Zenoff, O. Ordoñez, and M. E. Farías. 2008. “Occurrence of resistance to antibiotics, UV-B, and arsenic in bacteria isolated from extreme environments in high-altitude (above 4400 m) Andean Wetlands.” Curr. Microbiol. 56 (5): 510–517. https://doi.org/10.1007/s00284-008-9103-2.
Doyle, M. P. 1991. “Escherichia coli O157: H7 and its significance in foods.” Int. J. Food Microbiol. 12 (4): 289–301. https://doi.org/10.1016/0168-1605(91)90143-D.
Fernández Zenoff, V., F. Siñeriz, and M. E. Farias. 2006. “Diverse responses to UV-B radiation and repair mechanisms of bacteria isolated from high-altitude aquatic environments.” Appl. Environ. Microbiol. 72 (12): 7857–7863. https://doi.org/10.1128/AEM.01333-06.
Gayán, E., S. Condón, and I. Álvarez. 2014. “Continuous-flow UV liquid food pasteurization: Engineering aspects.” Food Bioprocess Technol. 7 (10): 2813–2827. https://doi.org/10.1007/s11947-014-1267-0.
Ghosh, D., B. Veeraraghavan, R. Elangovan, and P. Vivekanandan. 2020. “Antibiotic resistance and epigenetics: More to it than meets the eye.” Antimicrob. Agents Chemother. 64 (2): e02225-19. https://doi.org/10.1128/AAC.02225-19.
Gómez-López, V. M. 2012. “Continuous UV-C light.” Chap. 21 in Decontamination of fresh and minimally processed produce.
Kallen, A. J., Y. Mu, S. Bulens, A. Reingold, S. Petit, K. Gershman, S. M. Ray, L. H. Harrison, R. Lynfield, and G. Dumyati. 2010. “Health care–associated invasive MRSA infections, 2005–2008.” JAMA 304 (6): 641–647. https://doi.org/10.1001/jama.2010.1115.
Kester, J. C., and S. M. Fortune. 2014. “Persisters and beyond: Mechanisms of phenotypic drug resistance and drug tolerance in bacteria.” Crit. Rev. Biochem. Mol. Biol. 49 (2): 91–101. https://doi.org/10.3109/10409238.2013.869543.
Kitagawa, H., T. Nomura, T. Nazmul, K. Omori, N. Shigemoto, T. Sakaguchi, and H. Ohge. 2021. “Effectiveness of 222-nm ultraviolet light on disinfecting SARS-CoV-2 surface contamination.” Am. J. Infect. Control 49 (3): 299–301. https://doi.org/10.1016/j.ajic.2020.08.022.
Köck, R., et al. 2010. “Methicillin-resistant Staphylococcus aureus (MRSA): Burden of disease and control challenges in Europe.” Euro Surveillance 15 (41): 19688. https://doi.org/10.2807/ese.15.41.19688-en.
Kourtis, A. P., K. Hatfield, J. Baggs, Y. Mu, I. See, E. Epson, J. Nadle, M. A. Kainer, G. Dumyati, S. Petit, and S. M. Ray. 2019. “Vital signs: Epidemiology and recent trends in methicillin-resistant and in methicillin-susceptible Staphylococcus aureus bloodstream infections—United States.” MMWR Morb. Mortal Wkly. Rep. 68 (9): 214. https://doi.org/10.15585/mmwr.mm6809e1.
La Duc, M. T., A. Dekas, S. Osman, C. Moissl, D. Newcombe, and K. Venkateswaran. 2007. “Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments.” Appl. Environ. Microbiol. 73 (8): 2600–2611. https://doi.org/10.1128/AEM.03007-06.
Lim, J. Y., J. W. Yoon, and C. J. Hovde. 2010. “A brief overview of Escherichia coli O157:H7 and its plasmid O157.” J. Microbiol. Biotechnol. 20 (1): 5–14. https://doi.org/10.4014/jmb.0908.08007.
Luo, W., A. Chen, M. Chen, W. Dong, and X. Hou. 2014. “Comparison of sterilization efficiency of pulsed and continuous UV light using tunable frequency UV system.” Innovative Food Sci. Emerging Technol. 26 (Dec): 220–225. https://doi.org/10.1016/j.ifset.2014.10.002.
Maclean, M., K. McKenzie, J. G. Anderson, G. Gettinby, and S. J. MacGregor. 2014. “405 nm light technology for the inactivation of pathogens and its potential role for environmental disinfection and infection control.” J. Hosp. Infect. 88 (1): 1–11. https://doi.org/10.1016/j.jhin.2014.06.004.
Marizcurrena, J. J., M. A. Morel, V. Braña, D. Morales, W. Martinez-López, and S. Castro-Sowinski. 2017. “Searching for novel photolyases in UVC-resistant Antarctic bacteria.” Extremophiles 21 (2): 409–418. https://doi.org/10.1007/s00792-016-0914-y.
McDonald, R., S. Gupta, M. Maclean, P. Ramakrishnan, J. Anderson, S. MacGregor, D. Meek, and M. Grant. 2013. “405 nm light exposure of osteoblasts and inactivation of bacterial isolates from arthroplasty patients: Potential for new disinfection applications?” Eur. Cells Mater. 25 (Mar): 204–214. https://doi.org/10.22203/eCM.v025a15.
Muñoz, R. B., A. F. F. Giacobone, and O. J. Oppezzo. 2021. “Dose fractionation as a promising strategy to improve UV disinfection.” J. Photochem. Photobiol. 7 (Sep): 100034. https://doi.org/10.1016/j.jpap.2021.100034.
Narita, K., K. Asano, Y. Morimoto, T. Igarashi, M. R. Hamblin, T. Dai, and A. Nakane. 2018. “Disinfection and healing effects of 222-nm UVC light on methicillin-resistant Staphylococcus aureus infection in mouse wounds.” J. Photochem. Photobiol. B 178 (Jan): 10–18. https://doi.org/10.1016/j.jphotobiol.2017.10.030.
Osman, S., Z. Peeters, M. T. La Duc, R. Mancinelli, P. Ehrenfreund, and K. Venkateswaran. 2008. “Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation.” Appl. Environ. Microbiol. 74 (4): 959–970. https://doi.org/10.1128/AEM.01973-07.
Rani, A., V. B. Ravindran, A. Surapaneni, N. Mantri, and A. S. Ball. 2021. “Trends in point-of-care diagnosis for Escherichia coli O157:H7 in food and water.” Int. J. Food Microbiol. 349 (Jul): 109233. https://doi.org/10.1016/j.ijfoodmicro.2021.109233.
Rossitto, P., J. S. Cullor, J. Crook, J. Parko, P. Sechi, and B. Cenci-Goga. 2012. “Effects of UV irradiation in a continuous turbulent flow UV reactor on microbiological and sensory characteristics of cow’s milk.” J. Food Prot. 75 (12): 2197–2207. https://doi.org/10.4315/0362-028X.JFP-12-036.
Sandoval-Motta, S., and M. Aldana. 2016. “Adaptive resistance to antibiotics in bacteria: A systems biology perspective.” Wiley Interdiscip. Rev. Syst. Biol. Med. 8 (3): 253–267. https://doi.org/10.1002/wsbm.1335.
Shibai, A., Y. Takahashi, Y. Ishizawa, D. Motooka, S. Nakamura, B.-W. Ying, and S. Tsuru. 2017. “Mutation accumulation under UV radiation in Escherichia coli.” Sci. Rep. 7 (1): 1–12. https://doi.org/10.1038/s41598-017-15008-1.
Sholtes, K., and K. G. Linden. 2019. “Pulsed and continuous light UV LED: Microbial inactivation, electrical, and time efficiency.” Water Res. 165 (Nov): 114965. https://doi.org/10.1016/j.watres.2019.114965.
Stefani, S., D. R. Chung, J. A. Lindsay, A. W. Friedrich, A. M. Kearns, H. Westh, and F. M. MacKenzie. 2012. “Meticillin-resistant Staphylococcus aureus (MRSA): Global epidemiology and harmonisation of typing methods.” Int. J. Antimicrob. Agents 39 (4): 273–282. https://doi.org/10.1016/j.ijantimicag.2011.09.030.
Wang, D., T. Oppenländer, M. G. El-Din, and J. R. Bolton. 2010. “Comparison of the disinfection effects of vacuum-UV (VUV) and UV light on Bacillus subtilis spores in aqueous suspensions at 172, 222 and 254 nm.” Photochem. Photobiol. 86 (1): 176–181. https://doi.org/10.1111/j.1751-1097.2009.00640.x.
Yang, Y., S. Itahashi, S.-i. Yokobori, and A. Yamagishi. 2008. “UV-resistant bacteria isolated from upper troposphere and lower stratosphere.” Biol. Sci. Space 22 (1): 18–25. https://doi.org/10.2187/bss.22.18.

Information & Authors

Information

Published In

Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 149Issue 6June 2023

History

Received: Sep 22, 2022
Accepted: Jan 28, 2023
Published online: Apr 11, 2023
Published in print: Jun 1, 2023
Discussion open until: Sep 11, 2023

Permissions

Request permissions for this article.

ASCE Technical Topics:

Authors

Affiliations

Saeed Keshani Langroodi [email protected]
Bio Lab Director, AAPlasma LLC, 1325 S 33rd St., Philadelphia, PA 19146. Email: [email protected]
Christopher M. Sales [email protected]
Associate Professor, Dept. of Civil, Architectural, and Environmental Engineering, Drexel Univ., 3141 Chestnut St., Philadelphia, PA 19104. Email: [email protected]
Chetan Jinadatha [email protected]
Chief of Infectious Diseases Section, Central Texas Veterans Health Care System, 1901 Veterans Memorial Dr., Temple, TX 76504. Email: [email protected]
CEO, AAPlasma LLC, 1325 S 33rd St., Philadelphia, PA 19146 (corresponding author). ORCID: https://orcid.org/0000-0003-4006-4722. Email: [email protected]

Metrics & Citations

Metrics

Citations

Download citation

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

View Options

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share with email

Email a colleague

Share