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Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection

Helminth infection in pigs serves as an excellent model for the study of the interaction between human malnutrition and parasitic infection and could have important implications in human health. We had observed that pigs infected with Trichuris suis for 21 days showed significant changes in the prox...

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Autores principales: Wu, Sitao, Li, Robert W., Li, Weizhong, Beshah, Ethiopia, Dawson, Harry D., Urban, Joseph F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3332011/
https://www.ncbi.nlm.nih.gov/pubmed/22532855
http://dx.doi.org/10.1371/journal.pone.0035470
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author Wu, Sitao
Li, Robert W.
Li, Weizhong
Beshah, Ethiopia
Dawson, Harry D.
Urban, Joseph F.
author_facet Wu, Sitao
Li, Robert W.
Li, Weizhong
Beshah, Ethiopia
Dawson, Harry D.
Urban, Joseph F.
author_sort Wu, Sitao
collection PubMed
description Helminth infection in pigs serves as an excellent model for the study of the interaction between human malnutrition and parasitic infection and could have important implications in human health. We had observed that pigs infected with Trichuris suis for 21 days showed significant changes in the proximal colon microbiota. In this study, interactions between worm burden and severity of disruptions to the microbial composition and metabolic potentials in the porcine proximal colon microbiota were investigated using metagenomic tools. Pigs were infected by a single dose of T. suis eggs for 53 days. Among infected pigs, two cohorts were differentiated that either had adult worms or were worm-free. Infection resulted in a significant change in the abundance of approximately 13% of genera detected in the proximal colon microbiota regardless of worm status, suggesting a relatively persistent change over time in the microbiota due to the initial infection. A significant reduction in the abundance of Fibrobacter and Ruminococcus indicated a change in the fibrolytic capacity of the colon microbiota in T. suis infected pigs. In addition, ∼10% of identified KEGG pathways were affected by infection, including ABC transporters, peptidoglycan biosynthesis, and lipopolysaccharide biosynthesis as well as α-linolenic acid metabolism. Trichuris suis infection modulated host immunity to Campylobacter because there was a 3-fold increase in the relative abundance in the colon microbiota of infected pigs with worms compared to naïve controls, but a 3-fold reduction in worm-free infected pigs compared to controls. The level of pathology observed in infected pigs with worms compared to worm-free infected pigs may relate to the local host response because expression of several Th2-related genes were enhanced in infected pigs with worms versus those worm-free. Our findings provided insight into the dynamics of the proximal colon microbiota in pigs in response to T. suis infection.
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spelling pubmed-33320112012-04-24 Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection Wu, Sitao Li, Robert W. Li, Weizhong Beshah, Ethiopia Dawson, Harry D. Urban, Joseph F. PLoS One Research Article Helminth infection in pigs serves as an excellent model for the study of the interaction between human malnutrition and parasitic infection and could have important implications in human health. We had observed that pigs infected with Trichuris suis for 21 days showed significant changes in the proximal colon microbiota. In this study, interactions between worm burden and severity of disruptions to the microbial composition and metabolic potentials in the porcine proximal colon microbiota were investigated using metagenomic tools. Pigs were infected by a single dose of T. suis eggs for 53 days. Among infected pigs, two cohorts were differentiated that either had adult worms or were worm-free. Infection resulted in a significant change in the abundance of approximately 13% of genera detected in the proximal colon microbiota regardless of worm status, suggesting a relatively persistent change over time in the microbiota due to the initial infection. A significant reduction in the abundance of Fibrobacter and Ruminococcus indicated a change in the fibrolytic capacity of the colon microbiota in T. suis infected pigs. In addition, ∼10% of identified KEGG pathways were affected by infection, including ABC transporters, peptidoglycan biosynthesis, and lipopolysaccharide biosynthesis as well as α-linolenic acid metabolism. Trichuris suis infection modulated host immunity to Campylobacter because there was a 3-fold increase in the relative abundance in the colon microbiota of infected pigs with worms compared to naïve controls, but a 3-fold reduction in worm-free infected pigs compared to controls. The level of pathology observed in infected pigs with worms compared to worm-free infected pigs may relate to the local host response because expression of several Th2-related genes were enhanced in infected pigs with worms versus those worm-free. Our findings provided insight into the dynamics of the proximal colon microbiota in pigs in response to T. suis infection. Public Library of Science 2012-04-20 /pmc/articles/PMC3332011/ /pubmed/22532855 http://dx.doi.org/10.1371/journal.pone.0035470 Text en This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Wu, Sitao
Li, Robert W.
Li, Weizhong
Beshah, Ethiopia
Dawson, Harry D.
Urban, Joseph F.
Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title_full Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title_fullStr Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title_full_unstemmed Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title_short Worm Burden-Dependent Disruption of the Porcine Colon Microbiota by Trichuris suis Infection
title_sort worm burden-dependent disruption of the porcine colon microbiota by trichuris suis infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3332011/
https://www.ncbi.nlm.nih.gov/pubmed/22532855
http://dx.doi.org/10.1371/journal.pone.0035470
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