Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues

ABSTRACT Human astroviruses (HAstV) are among the most common causative agents of viral gastroenteritis, especially in children, and extraintestinal manifestations have also been described. These viruses are transmitted by the fecal-oral route, implying that stool composition and the gut microbiota...

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Autores principales:	Francisco J. Pérez-Rodriguez, Gael Vieille, Lara Turin, Soner Yildiz, Caroline Tapparel, Laurent Kaiser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	astrovirus enteric bacteria viral transmission virus and bacteria interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f749a188685d4dd69776c190f5396fee
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spelling	oai:doaj.org-article:f749a188685d4dd69776c190f5396fee2021-11-15T15:22:24ZFecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues10.1128/mSphere.00568-192379-5042https://doaj.org/article/f749a188685d4dd69776c190f5396fee2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00568-19https://doaj.org/toc/2379-5042ABSTRACT Human astroviruses (HAstV) are among the most common causative agents of viral gastroenteritis, especially in children, and extraintestinal manifestations have also been described. These viruses are transmitted by the fecal-oral route, implying that stool composition and the gut microbiota may impact their ability to remain infectious. For some enteric viruses, individual bacterial envelope components and other polysaccharide-containing molecules, which are abundant in stools, have been shown to enhance capsid stability. However, the role of the complex stool environment and, most importantly, the role of interindividual differences have been poorly studied. We used HAstV as a model to investigate how the stool environment in itself, its interindividual variability, and some specific stool components could affect HAstV stability and infectivity. Using two different HAstV genotypes, we found that stools as a whole modulate astrovirus infectivity not only in an individual-dependent manner but also in a manner that depends on the viral genotype. A virus-protective effect was observed after incubation with various Gram-positive and Gram-negative bacteria as well as with bacterial components, such as lipopolysaccharide and peptidoglycan. These results were further confirmed in human intestinal tissues, a more physiologically relevant system. Astrovirus infectivity was also preserved by mucin, a major component of intestinal mucus. We further confirmed that these components stabilize the viral capsid. These results show that although HAstV benefits from the stabilizing effect of fecal components, the complexity and variability of the stool composition and the multiple potential interactions may explain the interindividual differences in viral transmission observed in real life. IMPORTANCE To ensure transmission, enteric viruses must maintain their infectivity during the various environmental challenges that they face in transit within and between hosts. Increased knowledge of the factors affecting enteric virus survival may help to control their transmission. This study reveals that specific fecal bacterial components preserve classic human astrovirus infectivity by stabilizing viral particles. However, the outcomes of stool-virus interactions are very variable, ranging from protection to a reduction of viral infectivity, depending on the viral genotype and the individual from whom the stool has been collected. We show that the transmissibility of enteric viruses is dependent on the intestinal contents of the infected individual and highlight the complex multiple interactions that could explain the stochastic nature of enteric virus transmission in humans.Francisco J. Pérez-RodriguezGael VieilleLara TurinSoner YildizCaroline TapparelLaurent KaiserAmerican Society for Microbiologyarticleastrovirusenteric bacteriaviral transmissionvirus and bacteria interactionsMicrobiologyQR1-502ENmSphere, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	astrovirus enteric bacteria viral transmission virus and bacteria interactions Microbiology QR1-502
spellingShingle	astrovirus enteric bacteria viral transmission virus and bacteria interactions Microbiology QR1-502 Francisco J. Pérez-Rodriguez Gael Vieille Lara Turin Soner Yildiz Caroline Tapparel Laurent Kaiser Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
description	ABSTRACT Human astroviruses (HAstV) are among the most common causative agents of viral gastroenteritis, especially in children, and extraintestinal manifestations have also been described. These viruses are transmitted by the fecal-oral route, implying that stool composition and the gut microbiota may impact their ability to remain infectious. For some enteric viruses, individual bacterial envelope components and other polysaccharide-containing molecules, which are abundant in stools, have been shown to enhance capsid stability. However, the role of the complex stool environment and, most importantly, the role of interindividual differences have been poorly studied. We used HAstV as a model to investigate how the stool environment in itself, its interindividual variability, and some specific stool components could affect HAstV stability and infectivity. Using two different HAstV genotypes, we found that stools as a whole modulate astrovirus infectivity not only in an individual-dependent manner but also in a manner that depends on the viral genotype. A virus-protective effect was observed after incubation with various Gram-positive and Gram-negative bacteria as well as with bacterial components, such as lipopolysaccharide and peptidoglycan. These results were further confirmed in human intestinal tissues, a more physiologically relevant system. Astrovirus infectivity was also preserved by mucin, a major component of intestinal mucus. We further confirmed that these components stabilize the viral capsid. These results show that although HAstV benefits from the stabilizing effect of fecal components, the complexity and variability of the stool composition and the multiple potential interactions may explain the interindividual differences in viral transmission observed in real life. IMPORTANCE To ensure transmission, enteric viruses must maintain their infectivity during the various environmental challenges that they face in transit within and between hosts. Increased knowledge of the factors affecting enteric virus survival may help to control their transmission. This study reveals that specific fecal bacterial components preserve classic human astrovirus infectivity by stabilizing viral particles. However, the outcomes of stool-virus interactions are very variable, ranging from protection to a reduction of viral infectivity, depending on the viral genotype and the individual from whom the stool has been collected. We show that the transmissibility of enteric viruses is dependent on the intestinal contents of the infected individual and highlight the complex multiple interactions that could explain the stochastic nature of enteric virus transmission in humans.
format	article
author	Francisco J. Pérez-Rodriguez Gael Vieille Lara Turin Soner Yildiz Caroline Tapparel Laurent Kaiser
author_facet	Francisco J. Pérez-Rodriguez Gael Vieille Lara Turin Soner Yildiz Caroline Tapparel Laurent Kaiser
author_sort	Francisco J. Pérez-Rodriguez
title	Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
title_short	Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
title_full	Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
title_fullStr	Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
title_full_unstemmed	Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues
title_sort	fecal components modulate human astrovirus infectivity in cells and reconstituted intestinal tissues
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/f749a188685d4dd69776c190f5396fee
work_keys_str_mv	AT franciscojperezrodriguez fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues AT gaelvieille fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues AT laraturin fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues AT soneryildiz fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues AT carolinetapparel fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues AT laurentkaiser fecalcomponentsmodulatehumanastrovirusinfectivityincellsandreconstitutedintestinaltissues
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Fecal Components Modulate Human Astrovirus Infectivity in Cells and Reconstituted Intestinal Tissues

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