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Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile

The pathological mechanisms of gastrointestinal disorders, including inflammatory bowel disease (IBD), in pigs are poorly understood. We report the induction of intestinal inflammation in heat-stressed (HS) pigs, fecal microbiota transplantation from pigs to mice, and explain the role of microorgani...

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Autores principales: Hu, Canying, Patil, Yadnyavalkya, Gong, Dongliang, Yu, Tianyue, Li, Junyu, Wu, Lianyun, Liu, Xiaoxi, Yu, Zhichao, Ma, Xinbing, Yong, Yanhong, Chen, Jinjun, Gooneratne, Ravi, Ju, Xianghong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8921775/
https://www.ncbi.nlm.nih.gov/pubmed/35300220
http://dx.doi.org/10.3389/fvets.2022.686902
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author Hu, Canying
Patil, Yadnyavalkya
Gong, Dongliang
Yu, Tianyue
Li, Junyu
Wu, Lianyun
Liu, Xiaoxi
Yu, Zhichao
Ma, Xinbing
Yong, Yanhong
Chen, Jinjun
Gooneratne, Ravi
Ju, Xianghong
author_facet Hu, Canying
Patil, Yadnyavalkya
Gong, Dongliang
Yu, Tianyue
Li, Junyu
Wu, Lianyun
Liu, Xiaoxi
Yu, Zhichao
Ma, Xinbing
Yong, Yanhong
Chen, Jinjun
Gooneratne, Ravi
Ju, Xianghong
author_sort Hu, Canying
collection PubMed
description The pathological mechanisms of gastrointestinal disorders, including inflammatory bowel disease (IBD), in pigs are poorly understood. We report the induction of intestinal inflammation in heat-stressed (HS) pigs, fecal microbiota transplantation from pigs to mice, and explain the role of microorganisms in IBD. 24 adult pigs were subjected to HS (34 ± 1 °C; 75–85% relative humidity for 24h) while 24 control pigs (CP) were kept at 25 ± 3°C and the same humidity. Pigs were sacrificed on days 1, 7, 14, 21. Colonic content microbiome analyses were conducted. Pseudo-germ-free mice were fed by gavage with fecal microbiota from HS-pigs and CP to induce pig-like responses in mice. From 7 d, HS-pigs exhibited fever and diarrhea, and significantly lower colonic mucosal thickness, crypt depth/width, and goblet cell number. Compared with each control group, the concentration of cortisol in the peripheral blood of HS pigs gradually increased, significantly so on days 7, 14, and 21 (P < 0.01). While the concentration of LPS in HS pigs' peripheral blood was significantly higher on days 7, 14 (P < 0.01), and 21 (P < 0.05) compared with that of the control group. The colonic microbiome composition of HS-pigs was different to that of CP. By day 14, opportunistic pathogens (e.g., Campylobacterales) had increased in HS-pigs. The composition of the colonic microbiome in mice administered feces from HS-pigs was different from those receiving CP feces. Bacteroides were significantly diminished, Akkermansia were significantly increased, and intestinal damage and goblet cell numbers were higher in mice that received HS-pig feces. Moreover, we verified the relevance of differences in the microbiota of the colon among treatments. Heat stress promotes changes in gut microbiome composition, which can affect the colonic microbial structure of mice through fecal microbiota transplantation; the molecular mechanisms require further investigation. This study enhanced our understanding of stress-induced inflammation in the colon and the increase in diarrhea in mammals subjected to prolonged HS. Our results provide useful information for preventing or ameliorating deficits in pig production caused by prolonged exposure to high temperatures.
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spelling pubmed-89217752022-03-16 Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile Hu, Canying Patil, Yadnyavalkya Gong, Dongliang Yu, Tianyue Li, Junyu Wu, Lianyun Liu, Xiaoxi Yu, Zhichao Ma, Xinbing Yong, Yanhong Chen, Jinjun Gooneratne, Ravi Ju, Xianghong Front Vet Sci Veterinary Science The pathological mechanisms of gastrointestinal disorders, including inflammatory bowel disease (IBD), in pigs are poorly understood. We report the induction of intestinal inflammation in heat-stressed (HS) pigs, fecal microbiota transplantation from pigs to mice, and explain the role of microorganisms in IBD. 24 adult pigs were subjected to HS (34 ± 1 °C; 75–85% relative humidity for 24h) while 24 control pigs (CP) were kept at 25 ± 3°C and the same humidity. Pigs were sacrificed on days 1, 7, 14, 21. Colonic content microbiome analyses were conducted. Pseudo-germ-free mice were fed by gavage with fecal microbiota from HS-pigs and CP to induce pig-like responses in mice. From 7 d, HS-pigs exhibited fever and diarrhea, and significantly lower colonic mucosal thickness, crypt depth/width, and goblet cell number. Compared with each control group, the concentration of cortisol in the peripheral blood of HS pigs gradually increased, significantly so on days 7, 14, and 21 (P < 0.01). While the concentration of LPS in HS pigs' peripheral blood was significantly higher on days 7, 14 (P < 0.01), and 21 (P < 0.05) compared with that of the control group. The colonic microbiome composition of HS-pigs was different to that of CP. By day 14, opportunistic pathogens (e.g., Campylobacterales) had increased in HS-pigs. The composition of the colonic microbiome in mice administered feces from HS-pigs was different from those receiving CP feces. Bacteroides were significantly diminished, Akkermansia were significantly increased, and intestinal damage and goblet cell numbers were higher in mice that received HS-pig feces. Moreover, we verified the relevance of differences in the microbiota of the colon among treatments. Heat stress promotes changes in gut microbiome composition, which can affect the colonic microbial structure of mice through fecal microbiota transplantation; the molecular mechanisms require further investigation. This study enhanced our understanding of stress-induced inflammation in the colon and the increase in diarrhea in mammals subjected to prolonged HS. Our results provide useful information for preventing or ameliorating deficits in pig production caused by prolonged exposure to high temperatures. Frontiers Media S.A. 2022-03-01 /pmc/articles/PMC8921775/ /pubmed/35300220 http://dx.doi.org/10.3389/fvets.2022.686902 Text en Copyright © 2022 Hu, Patil, Gong, Yu, Li, Wu, Liu, Yu, Ma, Yong, Chen, Gooneratne and Ju. https://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 Veterinary Science
Hu, Canying
Patil, Yadnyavalkya
Gong, Dongliang
Yu, Tianyue
Li, Junyu
Wu, Lianyun
Liu, Xiaoxi
Yu, Zhichao
Ma, Xinbing
Yong, Yanhong
Chen, Jinjun
Gooneratne, Ravi
Ju, Xianghong
Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title_full Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title_fullStr Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title_full_unstemmed Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title_short Heat Stress-Induced Dysbiosis of Porcine Colon Microbiota Plays a Role in Intestinal Damage: A Fecal Microbiota Profile
title_sort heat stress-induced dysbiosis of porcine colon microbiota plays a role in intestinal damage: a fecal microbiota profile
topic Veterinary Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8921775/
https://www.ncbi.nlm.nih.gov/pubmed/35300220
http://dx.doi.org/10.3389/fvets.2022.686902
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