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Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways

Vibrio parahaemolyticus (Vp), a major food-borne pathogen, is responsible for severe infections such as gastroenteritis and septicemia, which may be accompanied by life-threatening complications. While studies have evaluated factors that affect the virulence of the pathogen, none have investigated t...

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Autores principales: Wang, Rundong, Deng, Yijia, Deng, Qi, Sun, Dongfang, Fang, Zhijia, Sun, Lijun, Wang, Yaling, Gooneratne, Ravi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7002474/
https://www.ncbi.nlm.nih.gov/pubmed/32082289
http://dx.doi.org/10.3389/fmicb.2020.00073
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author Wang, Rundong
Deng, Yijia
Deng, Qi
Sun, Dongfang
Fang, Zhijia
Sun, Lijun
Wang, Yaling
Gooneratne, Ravi
author_facet Wang, Rundong
Deng, Yijia
Deng, Qi
Sun, Dongfang
Fang, Zhijia
Sun, Lijun
Wang, Yaling
Gooneratne, Ravi
author_sort Wang, Rundong
collection PubMed
description Vibrio parahaemolyticus (Vp), a major food-borne pathogen, is responsible for severe infections such as gastroenteritis and septicemia, which may be accompanied by life-threatening complications. While studies have evaluated factors that affect the virulence of the pathogen, none have investigated the interaction of Vp with gut microbiota. To address this knowledge gap, we compared the effect of Vp on gut bacterial community structure, immunity, liver and kidney function, in pseudo germ-free (PGF) mice and normal (control) mice. Significant damage to the ileum was observed in normal mice compared with the PGF mice. The inflammatory factors IL-1β, IL-6, and TNF-α in normal mice were ∼2.5-fold higher than in the PGF mice, and liver (ALT, AST, ALP) and kidney (BUN) function indices were ∼1.6-fold higher. The Vp infection substantially reduced species composition and richness of the gut microbial communities. In particular, there was a shift in keystone taxa, from protective species of genera Bacteroides, Lactobacillus, Bifidobacterium, and Akkermansia in the gut of control mice to opportunistic pathogens Enterobacteriaceae, Proteus, Prevotella, and Sutterella in Vp-infected mice, thus affecting microbiota-related biological functions in the mice. Specifically, pathways involved in infectious diseases and ion channels were significantly augmented in infected mice, while the pathways involved in metabolism, digestion and cell growth declined. We propose that the normal mice are more prone to Vp infection because of the alteration in gut-microbe-mediated functions. All these effects reduce intestinal resistance, with marked damage to the gut lining and pathogen leakage into the blood culminating in liver and kidney damage. These findings greatly advance our understanding of the mechanisms underlying interactions between Vp, the gut microbiota and the infected host.
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spelling pubmed-70024742020-02-20 Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways Wang, Rundong Deng, Yijia Deng, Qi Sun, Dongfang Fang, Zhijia Sun, Lijun Wang, Yaling Gooneratne, Ravi Front Microbiol Microbiology Vibrio parahaemolyticus (Vp), a major food-borne pathogen, is responsible for severe infections such as gastroenteritis and septicemia, which may be accompanied by life-threatening complications. While studies have evaluated factors that affect the virulence of the pathogen, none have investigated the interaction of Vp with gut microbiota. To address this knowledge gap, we compared the effect of Vp on gut bacterial community structure, immunity, liver and kidney function, in pseudo germ-free (PGF) mice and normal (control) mice. Significant damage to the ileum was observed in normal mice compared with the PGF mice. The inflammatory factors IL-1β, IL-6, and TNF-α in normal mice were ∼2.5-fold higher than in the PGF mice, and liver (ALT, AST, ALP) and kidney (BUN) function indices were ∼1.6-fold higher. The Vp infection substantially reduced species composition and richness of the gut microbial communities. In particular, there was a shift in keystone taxa, from protective species of genera Bacteroides, Lactobacillus, Bifidobacterium, and Akkermansia in the gut of control mice to opportunistic pathogens Enterobacteriaceae, Proteus, Prevotella, and Sutterella in Vp-infected mice, thus affecting microbiota-related biological functions in the mice. Specifically, pathways involved in infectious diseases and ion channels were significantly augmented in infected mice, while the pathways involved in metabolism, digestion and cell growth declined. We propose that the normal mice are more prone to Vp infection because of the alteration in gut-microbe-mediated functions. All these effects reduce intestinal resistance, with marked damage to the gut lining and pathogen leakage into the blood culminating in liver and kidney damage. These findings greatly advance our understanding of the mechanisms underlying interactions between Vp, the gut microbiota and the infected host. Frontiers Media S.A. 2020-01-30 /pmc/articles/PMC7002474/ /pubmed/32082289 http://dx.doi.org/10.3389/fmicb.2020.00073 Text en Copyright © 2020 Wang, Deng, Deng, Sun, Fang, Sun, Wang and Gooneratne. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wang, Rundong
Deng, Yijia
Deng, Qi
Sun, Dongfang
Fang, Zhijia
Sun, Lijun
Wang, Yaling
Gooneratne, Ravi
Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title_full Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title_fullStr Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title_full_unstemmed Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title_short Vibrio parahaemolyticus Infection in Mice Reduces Protective Gut Microbiota, Augmenting Disease Pathways
title_sort vibrio parahaemolyticus infection in mice reduces protective gut microbiota, augmenting disease pathways
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7002474/
https://www.ncbi.nlm.nih.gov/pubmed/32082289
http://dx.doi.org/10.3389/fmicb.2020.00073
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