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Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation

BACKGROUND: Heat stress (HS) jeopardizes intestinal barrier functions and augments intestinal permeability in pigs. However, whether HS-induced maternal microbial and metabolic changes in primiparous sows during late gestation remains elusive. We present here, a study investigating the fecal microbi...

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Autores principales: He, Jianwen, Guo, Huiduo, Zheng, Weijiang, Xue, Yongqiang, Zhao, Ruqian, Yao, Wen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6827230/
https://www.ncbi.nlm.nih.gov/pubmed/31700622
http://dx.doi.org/10.1186/s40104-019-0391-0
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author He, Jianwen
Guo, Huiduo
Zheng, Weijiang
Xue, Yongqiang
Zhao, Ruqian
Yao, Wen
author_facet He, Jianwen
Guo, Huiduo
Zheng, Weijiang
Xue, Yongqiang
Zhao, Ruqian
Yao, Wen
author_sort He, Jianwen
collection PubMed
description BACKGROUND: Heat stress (HS) jeopardizes intestinal barrier functions and augments intestinal permeability in pigs. However, whether HS-induced maternal microbial and metabolic changes in primiparous sows during late gestation remains elusive. We present here, a study investigating the fecal microbial and metabolic responses in late gestational primiparous sows when exposed to HS. METHODS: Twelve first-parity Landrace × Large White F1 sows were randomly assigned into two environmental treatments including the thermoneutral (TN) (18–22 °C; n = 6) and HS (28–32 °C; n = 6) conditions. Both treatments were applied from 85 d of gestation to farrowing. The serum and feces samples were collected on d 107 of gestation, for analyses including intestinal integrity biomarkers, high-throughput sequencing metagenomics, short-chain fatty acid (SCFA) profiles and nontargeted metabolomics. RESULTS: Our results show that HS group has higher serum Heat shock protein 70 (HSP70), lipopolysaccharide (LPS) and lipopolysaccharide-binding protein (LBP) levels. The gut microbial community can be altered upon HS by using β-diversity and taxon-based analysis. In particular, the relative abundance of genera and operational taxonomic units (OTUs) related to Clostridiales and Halomonas are higher in HS group, the relative abundance of genera and OTUs related to Bacteroidales and Streptococcus, however, are lower in HS group. Results of metabolic analysis reveal that HS lowers the concentrations of propionate, butyrate, total SCFA, succinate, fumarate, malate, lactate, aspartate, ethanolamine, β-alanine and niacin, whereas that of fructose and azelaic acid are higher in HS group. These metabolites mainly affect propanoate metabolism, alanine, aspartate and glutamate metabolism, phenylalanine metabolism, β-alanine metabolism, pantothenate and CoA biosynthesis, tricarboxylic acid cycle (TCA) and nicotinate and nicotinamide metabolism. Additionally, correlation analysis between significant microbes and metabolites indicated that the HS-induced microbiota shift is likely the cause of changes of intestinal metabolism. CONCLUSIONS: Taken together, we reveal characteristic structural and metabolic changes in maternal gut microbiota as a result of late gestational HS, which could potentially provide the basis for further study on offspring gut microbiota and immune programming.
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spelling pubmed-68272302019-11-07 Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation He, Jianwen Guo, Huiduo Zheng, Weijiang Xue, Yongqiang Zhao, Ruqian Yao, Wen J Anim Sci Biotechnol Research BACKGROUND: Heat stress (HS) jeopardizes intestinal barrier functions and augments intestinal permeability in pigs. However, whether HS-induced maternal microbial and metabolic changes in primiparous sows during late gestation remains elusive. We present here, a study investigating the fecal microbial and metabolic responses in late gestational primiparous sows when exposed to HS. METHODS: Twelve first-parity Landrace × Large White F1 sows were randomly assigned into two environmental treatments including the thermoneutral (TN) (18–22 °C; n = 6) and HS (28–32 °C; n = 6) conditions. Both treatments were applied from 85 d of gestation to farrowing. The serum and feces samples were collected on d 107 of gestation, for analyses including intestinal integrity biomarkers, high-throughput sequencing metagenomics, short-chain fatty acid (SCFA) profiles and nontargeted metabolomics. RESULTS: Our results show that HS group has higher serum Heat shock protein 70 (HSP70), lipopolysaccharide (LPS) and lipopolysaccharide-binding protein (LBP) levels. The gut microbial community can be altered upon HS by using β-diversity and taxon-based analysis. In particular, the relative abundance of genera and operational taxonomic units (OTUs) related to Clostridiales and Halomonas are higher in HS group, the relative abundance of genera and OTUs related to Bacteroidales and Streptococcus, however, are lower in HS group. Results of metabolic analysis reveal that HS lowers the concentrations of propionate, butyrate, total SCFA, succinate, fumarate, malate, lactate, aspartate, ethanolamine, β-alanine and niacin, whereas that of fructose and azelaic acid are higher in HS group. These metabolites mainly affect propanoate metabolism, alanine, aspartate and glutamate metabolism, phenylalanine metabolism, β-alanine metabolism, pantothenate and CoA biosynthesis, tricarboxylic acid cycle (TCA) and nicotinate and nicotinamide metabolism. Additionally, correlation analysis between significant microbes and metabolites indicated that the HS-induced microbiota shift is likely the cause of changes of intestinal metabolism. CONCLUSIONS: Taken together, we reveal characteristic structural and metabolic changes in maternal gut microbiota as a result of late gestational HS, which could potentially provide the basis for further study on offspring gut microbiota and immune programming. BioMed Central 2019-11-04 /pmc/articles/PMC6827230/ /pubmed/31700622 http://dx.doi.org/10.1186/s40104-019-0391-0 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
He, Jianwen
Guo, Huiduo
Zheng, Weijiang
Xue, Yongqiang
Zhao, Ruqian
Yao, Wen
Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title_full Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title_fullStr Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title_full_unstemmed Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title_short Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
title_sort heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6827230/
https://www.ncbi.nlm.nih.gov/pubmed/31700622
http://dx.doi.org/10.1186/s40104-019-0391-0
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