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Applied and Environmental Microbiology
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Public and Environmental Health Microbiology

Free-Chlorine Disinfection as a Selection Pressure on Norovirus

Andri Taruna Rachmadi, Masaaki Kitajima, Kozo Watanabe, Sakiko Yaegashi, Joeselle Serrana, Arata Nakamura, Toyoko Nakagomi, Osamu Nakagomi, Kazuhiko Katayama, Satoshi Okabe, Daisuke Sano
Christopher A. Elkins, Editor
Andri Taruna Rachmadi
Division of Environmental Engineering, Hokkaido University, Sapporo, Hokkaido, JapanDepartment of Civil and Environmental Engineering, Tohoku University, Sendai, Miyagi, Japan
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  • ORCID record for Andri Taruna Rachmadi
Masaaki Kitajima
Division of Environmental Engineering, Hokkaido University, Sapporo, Hokkaido, Japan
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Kozo Watanabe
Department of Civil and Environmental Engineering, Ehime University, Matsuyama, Ehime, Japan
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Sakiko Yaegashi
Department of Civil and Environmental Engineering, Ehime University, Matsuyama, Ehime, JapanDepartment of Civil and Environmental Engineering, University of Yamanashi, Kofu, Yamanashi, Japan
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Joeselle Serrana
Department of Civil and Environmental Engineering, Ehime University, Matsuyama, Ehime, Japan
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Arata Nakamura
Division of Environmental Engineering, Hokkaido University, Sapporo, Hokkaido, Japan
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Toyoko Nakagomi
Department of Molecular Microbiology and Immunology, Nagasaki University, Nagasaki, Japan
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Osamu Nakagomi
Department of Molecular Microbiology and Immunology, Nagasaki University, Nagasaki, Japan
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Kazuhiko Katayama
Laboratory of Viral Infection I, Department of Infection Control and Immunology, Kitasato Institute for Life Sciences, Kitasato University, Tokyo, Japan
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Satoshi Okabe
Division of Environmental Engineering, Hokkaido University, Sapporo, Hokkaido, Japan
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Daisuke Sano
Department of Civil and Environmental Engineering, Tohoku University, Sendai, Miyagi, JapanGraduate School of Environmental Studies, Tohoku University, Sendai, Miyagi, Japan
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Christopher A. Elkins
Centers for Disease Control and Prevention
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DOI: 10.1128/AEM.00244-18
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ABSTRACT

Human noroviruses are excreted in feces from infected individuals and included in wastewater. It is critical to remove/inactivate them in wastewater treatment processes, particularly in the disinfection step, before release to aquatic environments. However, the high mutation rates of human noroviruses raise concerns about the emergence of strains that are less susceptible to disinfectants and can survive even after wastewater treatment. This study aimed to demonstrate the strain-dependent susceptibility of norovirus to free chlorine. A population originated from the murine norovirus strain S7-PP3, a surrogate for human noroviruses in environmental testing, was exposed to free chlorine and then propagated in a host cell. This cycle of free chlorine exposure followed by propagation in cells was repeated 10 times, and populations with lower susceptibility to free chlorine were obtained from two independent trials of chlorine exposure cycles. Open reading frame 2 (ORF2) and ORF3 of the murine norovirus genome were analyzed by next-generation sequencing, and a unique nonsynonymous mutation (corresponding to a change from phenylalanine to serine) at nucleotide (nt) 7280 in ORF3, which encodes the minor capsid protein VP2, was found in chlorine-exposed populations from both trials. It was confirmed that all of the clones from the chlorine-treated population had lower susceptibility to free chlorine than those from the control population. These results indicate that exposure to free chlorine and dilution exert different driving forces to form murine norovirus (MNV) quasispecies, and that there is a selective force to form MNV quasispecies under free chlorine exposure.

IMPORTANCE This study showed that free chlorine disinfection exerted a selection pressure for murine norovirus (MNV). The strain-dependent viral susceptibility to the disinfectant elucidated in this study highlights the importance of employing less susceptible strains as representative viruses in disinfection tests, because the disinfection rate values obtained from more susceptible strains would be less useful in predicting the virus inactivation efficiency of circulating strains under practical disinfection conditions.

FOOTNOTES

    • Received 30 January 2018.
    • Accepted 20 April 2018.
    • Accepted manuscript posted online 27 April 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.00244-18.

  • Copyright © 2018 Rachmadi et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Free-Chlorine Disinfection as a Selection Pressure on Norovirus
Andri Taruna Rachmadi, Masaaki Kitajima, Kozo Watanabe, Sakiko Yaegashi, Joeselle Serrana, Arata Nakamura, Toyoko Nakagomi, Osamu Nakagomi, Kazuhiko Katayama, Satoshi Okabe, Daisuke Sano
Applied and Environmental Microbiology Jun 2018, 84 (13) e00244-18; DOI: 10.1128/AEM.00244-18

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Free-Chlorine Disinfection as a Selection Pressure on Norovirus
Andri Taruna Rachmadi, Masaaki Kitajima, Kozo Watanabe, Sakiko Yaegashi, Joeselle Serrana, Arata Nakamura, Toyoko Nakagomi, Osamu Nakagomi, Kazuhiko Katayama, Satoshi Okabe, Daisuke Sano
Applied and Environmental Microbiology Jun 2018, 84 (13) e00244-18; DOI: 10.1128/AEM.00244-18
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KEYWORDS

free chlorine
genetic drift
mutation
Norovirus
selection
susceptibility

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