Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status

ABSTRACT Intestinal microbiota composition and gut-associated immune response can contribute to the toxicity of arsenic. We investigated the potential toxicity of short-term arsenic exposure on gut microbiome composition, intestinal immune status, microbial arsenic resistance gene, and arsenic metab...

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Autores principales:	Kuppan Gokulan, Matthew G. Arnold, Jake Jensen, Michelle Vanlandingham, Nathan C. Twaddle, Daniel R. Doerge, Carl E. Cerniglia, Sangeeta Khare
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	arsenic arsenic resistance genes arsenic speciation developmental toxicity immune response intestinal microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a705a27fc34149fab82d483c7b6fb653
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spelling	oai:doaj.org-article:a705a27fc34149fab82d483c7b6fb6532021-11-15T16:00:15ZExposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status10.1128/mBio.01418-182150-7511https://doaj.org/article/a705a27fc34149fab82d483c7b6fb6532018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01418-18https://doaj.org/toc/2150-7511ABSTRACT Intestinal microbiota composition and gut-associated immune response can contribute to the toxicity of arsenic. We investigated the potential toxicity of short-term arsenic exposure on gut microbiome composition, intestinal immune status, microbial arsenic resistance gene, and arsenic metabolic profiles in adult and developmental stages of CD-1 mice. The potential toxicity of arsenite [As(III)] was determined for two life stages: (i) adult animals at 24 or 48 h after single gavage (0.05 mg/kg body weight [b.w.] [low dose], 0.1 mg/kg b.w. [medium dose], and 0.2 mg/kg b.w. [high dose]) and repeated exposure at 1 mg/liter for 8 days and (ii) postnatal day 10 (PND10) and PND21 after single gavage (0.05 mg/kg b.w.). Dose- and time-dependent responses in bacterial recovery/microbial composition were observed in adults after a single gavage. Repeated exposure caused a transient decrease in the recovery of intestinal bacteria, a shift in the bacterial population with abundance of arsenic resistance genes, and evidence for host metabolism of arsenite into less-reactive trivalent methylated species. Arsenic exposure in adult animals induced high levels of CC chemokines and of proinflammatory and anti-inflammatory cytokine secretion in intestine. Arsenic exposure at PND21 resulted in the development of distinct bacterial populations. Results of this study highlight significant changes in the intestinal microbiome and gut-associated immune status during a single or repeated exposure to arsenic in juvenile and adult animals. The data warrant investigation of the long-term effects of oral arsenic exposure on the microbiome and of immune system development and responses. IMPORTANCE Transformation of organic arsenic to toxic inorganic arsenic (iAs) is likely carried out by intestinal bacteria, and iAs may alter the viability of certain microbial populations. This study addressed the impact of arsenic exposure on intestinal microbiota diversity and host gut-associated immune mediators during early development or adulthood using scenarios of acute or repeated doses. During acute arsenic exposure, animals developed defense functions characterized by higher abundances of bacteria that are involved in arsenic resistance or detoxification mechanisms. Arsenite had a negative effect on the abundance of bacterial species that are involved in the conversion of protein to butyrate, which is an alternative energy source in the intestine. The intestinal mucosal immune cytokine profile reflected a mechanism of protection from arsenic toxicity.Kuppan GokulanMatthew G. ArnoldJake JensenMichelle VanlandinghamNathan C. TwaddleDaniel R. DoergeCarl E. CernigliaSangeeta KhareAmerican Society for Microbiologyarticlearsenicarsenic resistance genesarsenic speciationdevelopmental toxicityimmune responseintestinal microbiomeMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	arsenic arsenic resistance genes arsenic speciation developmental toxicity immune response intestinal microbiome Microbiology QR1-502
spellingShingle	arsenic arsenic resistance genes arsenic speciation developmental toxicity immune response intestinal microbiome Microbiology QR1-502 Kuppan Gokulan Matthew G. Arnold Jake Jensen Michelle Vanlandingham Nathan C. Twaddle Daniel R. Doerge Carl E. Cerniglia Sangeeta Khare Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
description	ABSTRACT Intestinal microbiota composition and gut-associated immune response can contribute to the toxicity of arsenic. We investigated the potential toxicity of short-term arsenic exposure on gut microbiome composition, intestinal immune status, microbial arsenic resistance gene, and arsenic metabolic profiles in adult and developmental stages of CD-1 mice. The potential toxicity of arsenite [As(III)] was determined for two life stages: (i) adult animals at 24 or 48 h after single gavage (0.05 mg/kg body weight [b.w.] [low dose], 0.1 mg/kg b.w. [medium dose], and 0.2 mg/kg b.w. [high dose]) and repeated exposure at 1 mg/liter for 8 days and (ii) postnatal day 10 (PND10) and PND21 after single gavage (0.05 mg/kg b.w.). Dose- and time-dependent responses in bacterial recovery/microbial composition were observed in adults after a single gavage. Repeated exposure caused a transient decrease in the recovery of intestinal bacteria, a shift in the bacterial population with abundance of arsenic resistance genes, and evidence for host metabolism of arsenite into less-reactive trivalent methylated species. Arsenic exposure in adult animals induced high levels of CC chemokines and of proinflammatory and anti-inflammatory cytokine secretion in intestine. Arsenic exposure at PND21 resulted in the development of distinct bacterial populations. Results of this study highlight significant changes in the intestinal microbiome and gut-associated immune status during a single or repeated exposure to arsenic in juvenile and adult animals. The data warrant investigation of the long-term effects of oral arsenic exposure on the microbiome and of immune system development and responses. IMPORTANCE Transformation of organic arsenic to toxic inorganic arsenic (iAs) is likely carried out by intestinal bacteria, and iAs may alter the viability of certain microbial populations. This study addressed the impact of arsenic exposure on intestinal microbiota diversity and host gut-associated immune mediators during early development or adulthood using scenarios of acute or repeated doses. During acute arsenic exposure, animals developed defense functions characterized by higher abundances of bacteria that are involved in arsenic resistance or detoxification mechanisms. Arsenite had a negative effect on the abundance of bacterial species that are involved in the conversion of protein to butyrate, which is an alternative energy source in the intestine. The intestinal mucosal immune cytokine profile reflected a mechanism of protection from arsenic toxicity.
format	article
author	Kuppan Gokulan Matthew G. Arnold Jake Jensen Michelle Vanlandingham Nathan C. Twaddle Daniel R. Doerge Carl E. Cerniglia Sangeeta Khare
author_facet	Kuppan Gokulan Matthew G. Arnold Jake Jensen Michelle Vanlandingham Nathan C. Twaddle Daniel R. Doerge Carl E. Cerniglia Sangeeta Khare
author_sort	Kuppan Gokulan
title	Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
title_short	Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
title_full	Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
title_fullStr	Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
title_full_unstemmed	Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status
title_sort	exposure to arsenite in cd-1 mice during juvenile and adult stages: effects on intestinal microbiota and gut-associated immune status
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/a705a27fc34149fab82d483c7b6fb653
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Exposure to Arsenite in CD-1 Mice during Juvenile and Adult Stages: Effects on Intestinal Microbiota and Gut-Associated Immune Status

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