Inactivation Mechanisms of Human and Animal Rotaviruses by Solar
UVA and Visible Light
Elbashir Araud,*
,†
Joanna L. Shisler,
‡
and Thanh H. Nguyen
†
†
Department of Civil and Environmental Engineering, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United
States
‡
Department of Microbiology and Department of Pathobiology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801,
United States
* S Supporting Information
ABSTRACT: Two rotavirus (RV) strains (sialidase-resistant Wa
and sialidase-sensitive OSU) were irradiated with simulated solar
UVA and visible light in sensitizer-free phosphate buffered solution
(PBS) (lacking exogenous reactive oxygen species (ROS)) or
secondary effluent wastewater (producing ROS). Although light
attenuated for up to 15% through the secondary effluent
wastewater (SEW), the inactivation efficacies increased by 0.7
log
10
for Wa and 2 log
10
for OSU compared to those in sensitizer-
free phosphate buffered solution (PBS) after 4 h of irradiation. A
binding assay using magnetic beads coated with porcine gastric
mucin containing receptors for rotaviruses (PGM-MB) was
developed to determine if inactivation influenced RV binding to
its receptors. The linear correlation between the reduction in
infectivity and the reduction in binding after irradiation in
sensitizer-free solution suggests that the main mechanism of RV inactivation in the absence of exogenous ROS was due to
damage to VP8*, the RV protein that binds to host cell receptors. For a given reduction in infectivity, greater damage in VP8*
was observed with sialidase-resistant Wa compared to sialidase-sensitive OSU. The lack of correlation between the reduction in
infectivity and the reduction in binding, in SEW, led us to include RNase treatment before the binding step to quantify virions
with intact protein capsids and exclude virions that can bind to the receptors but have their capsid permeable after irradiation.
This assay showed a linear correlation between the reduction in RV infectivity and RV-receptor interactions, suggesting that RV
inactivation in SEW was due to compromised capsid proteins other than the VP8* protein. Thus, rotavirus inactivation by UVA
and visible light irradiation depends on both the formation of ROS and the stability of viral proteins.
■
INTRODUCTION
Group A rotaviruses (RVs) are the major etiological agent of
acute gastroenteritis in infants worldwide and accounted for
215 000 deaths in children in 2013.
1
They have a low infectious
dose of fewer than 10 particles, and they shed at high titers
(10
10
-10
12
particles per gram of stool) from infected persons.
2-4
Despite the success of vaccines against RVs in the reduction of
severe gastroenteritis among infants, RVs are still of major public
health importance and the leading cause of diarrhea in children
younger than five years old, globally.
2,5
RV outbreaks still occur
worldwide due to the high genetic diversity of RVs and the lack of
cross-protection.
2,5
There are eight groups of RVs referred to as
A, B, C, D, E, F, G, and H. Humans are primarily infected by the
group A RV, which can be further divided into different
serotypes.
6
The outer capsid glycoprotein (VP7) and the spike
protein (VP4) differentiate RVs into 14 G (glycoprotein)
serotypes and 27 different P (protease sensitive) genotypes.
6
Currently, five serotypes (G1-G4, and G9) are the predominant
circulating viruses, accounting for almost 95% of strains
worldwide.
7
In addition, reassortment of RV strains between
animal and human has been reported.
8-13
Thus, RVs are highly
diverse, both antigenically and genetically.
RV-contaminated water and food are the main source of RV
outbreaks.
14
In both developed and developing countries,
infectious particles or genomes of human or animal RV are
found in drinking water sources.
15-19
The contamination of the
drinking water source is attributed to inadequately treated
wastewater.
20
Also, it is troublesome that RV is detected on
lettuce irrigated with surface water in the US.
21
Thus, the risk of
RV outbreaks may increase when contaminated surface water
comes into contact with vegetables and seafood. To complicate
matters, newly emerging RV strains due to intragenogroup
reassortment are reported constantly and may also add to current
or future RV outbreaks.
8,22
Therefore, prevention of RV
infection and outbreaks can be achieved by improving waste-
Received: December 20, 2017
Revised: April 13, 2018
Accepted: April 19, 2018
Published: April 19, 2018
Article
pubs.acs.org/est
Cite This: Environ. Sci. Technol. 2018, 52, 5682-5690
© 2018 American Chemical Society 5682 DOI: 10.1021/acs.est.7b06562
Environ. Sci. Technol. 2018, 52, 5682-5690
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