Experimental adaptation of human echovirus 11 to ultraviolet radiation leads to resistance to disinfection and ribavirin

Carratalà, Anna; Shim, Hyunjin; Zhong, Qingxia; Bachmann, Virginie; Jensen, Jeffrey D.; Kohn, Tamar

doi:10.1093/ve/vex035

Cited by 35 publications

(24 citation statements)

References 57 publications

(66 reference statements)

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“…If this is also the case for human noroviruses, it is important to use less susceptible (stronger) strains in a water disinfection test for estimating the virus inactivation rate; otherwise, the disinfection efficiency in an actual setting does not reach the expected level and an infection risk is posed even with disinfected water. The strain-dependent susceptibility of RNA viruses to a variety of disinfection technologies, including ozonation and UV light irradiation, and the possibilities of cross-resistance with other disinfectant and or antivirals which have been described previously ( 41 , 42 ) need to be further investigated to achieve safer usage of water that may be contaminated by pathogenic viruses.…”

Section: Discussionmentioning

confidence: 99%

Free-Chlorine Disinfection as a Selection Pressure on Norovirus

Rachmadi

Kitajima

Watanabe

et al. 2018

Appl Environ Microbiol

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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.

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Section: Discussionmentioning

confidence: 99%

Free-Chlorine Disinfection as a Selection Pressure on Norovirus

Rachmadi

Kitajima

Watanabe

et al. 2018

Appl Environ Microbiol

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“…RNA viruses rapidly evolve and therefore viruses with resistance to antiviral agents and disinfectants can arise when viruses are repeatedly exposed to sub-lethal doses of these agents (Carratalà et al, 2017, Bates et al, 1977a, Feigelstock et al, 2011, Foll et al, 2014, Hué et al, 2009, Irwin et al, 2016, Zhong et al, 2016, Zhong et al, 2017. PDI is an efficient antiviral agent for viral control, with only one study reporting an attempt to select PDI-resistant viruses (Costa et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…Studies have reported on the emergence of resistant viruses upon continuous administration of antiviral drugs and exposure to common water disinfectants e.g. resistance of HIV to antiretroviral drugs (Hué et al, 2009), influenza virus to oseltamivir (Foll et al, 2014), hepatitis C virus to ribavirin (Feigelstock et al, 2011), bacteriophage MS2 and human echovirus 11 to chlorine dioxide (ClO2) (Zhong et al, 2016, Zhong et al, 2017, poliovirus and bacteriophage F116 to free chlorine (Bates et al, 1977b, Payment et al, 1985 and human echovirus 11 to Ultraviolet C (UVC) (Carratalà et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Photodynamic inactivation of non-enveloped RNA viruses

Majiya

Adeyemi

Herod

et al. 2018

Journal of Photochemistry and Photobiology B: Biology

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“…Culturing and enumeration of viruses and phages. Echovirus 11 (E11) (Gregory strain, ATCC VR737) and adenovirus 2 (HAdV2; kindly provided by Rosina Girones, University of Barcelona) stocks were produced by infecting subconfluent monolayers of BGMK (kindly provided by Spiez Laboratory, Switzerland) and A549 cells (kindly provided by Rosina Girones, University of Barcelona), respectively, as described previously (35). Both cell lines were maintained at 37°C in 5% CO 2 with modified Eagle medium (MEM; Gibco, Frederick, MD), supplemented with 1% penicillin-streptomycin (Gibco, Frederick, MD) and 10% (growth medium) or 2% (maintenance medium) heat-inactivated fetal bovine serum (FBS; Gibco, Frederick, MD).…”

Section: Methodsmentioning

confidence: 99%

Control of Waterborne Human Viruses by Indigenous Bacteria and Protists Is Influenced by Temperature, Virus Type, and Microbial Species

Olive

Gan

Carratalà

et al. 2020

Appl Environ Microbiol

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Human viruses are ubiquitous contaminants in surface waters, where they can persist over extended periods of time. Among the factors governing their environmental persistence, the control (removal or inactivation) by microorganisms remains poorly understood. Here, we determined the contribution of indigenous bacteria and protists to the decay of human viruses in surface waters. Incubation of echovirus 11 (E11) in freshwater from Lake Geneva and seawater from the Mediterranean Sea led to a 2.5-log10 reduction in the infectious virus concentration within 48 h at 22°C, whereas E11 was stable in sterile controls. The observed virus reduction was attributed to the action of both bacteria and protists in the biologically active matrices. The effect of microorganisms on viruses was temperature dependent, with a complete inhibition of microbial virus control in lake water at temperatures of ≤16°C. Among three protist isolates tested (Paraphysomonas sp., Uronema marinum, and Caecitellus paraparvulus), Caecitellus paraparvulus was particularly efficient at controlling E11 (2.1-log10 reduction over 4 days with an initial protist concentration of 103 cells ml−1). In addition, other viruses (human adenovirus type 2 and bacteriophage H6) exhibited different grazing kinetics than E11, indicating that the efficacy of antiviral action also depended on the type of virus. In conclusion, indigenous bacteria and protists in lake water and seawater can modulate the persistence of E11. These results pave the way for further research to understand how microorganisms control human viral pathogens in aquatic ecosystems and to exploit this process as a treatment solution to enhance microbial water safety. IMPORTANCE Waterborne human viruses can persist in the environment, causing a risk to human health over long periods of time. In this work, we demonstrate that in both freshwater and seawater environments, indigenous bacteria and protists can graze on waterborne viruses and thereby reduce their persistence. We furthermore demonstrate that the efficiency of the grazing process depends on temperature, virus type, and protist species. These findings may facilitate the design of biological methods for the disinfection of water and wastewater.

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Experimental adaptation of human echovirus 11 to ultraviolet radiation leads to resistance to disinfection and ribavirin

Cited by 35 publications

References 57 publications

Free-Chlorine Disinfection as a Selection Pressure on Norovirus

Free-Chlorine Disinfection as a Selection Pressure on Norovirus

Photodynamic inactivation of non-enveloped RNA viruses

Control of Waterborne Human Viruses by Indigenous Bacteria and Protists Is Influenced by Temperature, Virus Type, and Microbial Species

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