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Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)

The present study aimed at investigating the impact of heat challenges on gut microbiota composition in growing pigs and its relationship with pigs’ performance and thermoregulation responses. From a total of 10 F1 sire families, 558 and 564 backcross Large White × Créole pigs were raised and phenot...

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Autores principales: Le Sciellour, Mathilde, Zemb, Olivier, Hochu, Isabelle, Riquet, Juliette, Gilbert, Hélène, Giorgi, Mario, Billon, Yvon, Gourdine, Jean-Luc, Renaudeau, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6735821/
https://www.ncbi.nlm.nih.gov/pubmed/31268142
http://dx.doi.org/10.1093/jas/skz222
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author Le Sciellour, Mathilde
Zemb, Olivier
Hochu, Isabelle
Riquet, Juliette
Gilbert, Hélène
Giorgi, Mario
Billon, Yvon
Gourdine, Jean-Luc
Renaudeau, David
author_facet Le Sciellour, Mathilde
Zemb, Olivier
Hochu, Isabelle
Riquet, Juliette
Gilbert, Hélène
Giorgi, Mario
Billon, Yvon
Gourdine, Jean-Luc
Renaudeau, David
author_sort Le Sciellour, Mathilde
collection PubMed
description The present study aimed at investigating the impact of heat challenges on gut microbiota composition in growing pigs and its relationship with pigs’ performance and thermoregulation responses. From a total of 10 F1 sire families, 558 and 564 backcross Large White × Créole pigs were raised and phenotyped from 11 to 23 wk of age in temperate (TEMP) and in tropical (TROP) climates, respectively. In TEMP, all pigs were subjected to an acute heat challenge (3 wk at 29 °C) from 23 to 26 wk of age. Feces samples were collected at 23 wk of age both in TEMP and TROP climate (TEMP23 and TROP23 samples, respectively) and at 26 wk of age in TEMP climate (TEMP26 samples) for 16S rRNA analyses of fecal microbiota composition. The fecal microbiota composition significantly differed between the 3 environments. Using a generalized linear model on microbiota composition, 182 operational taxonomic units (OTU) and 2 pathways were differentially abundant between TEMP23 and TEMP26, and 1,296 OTU and 20 pathways between TEMP23 and TROP23. Using fecal samples collected at 23 wk of age, pigs raised under the 2 climates were discriminated with 36 OTU using a sparse partial least square discriminant analysis that had a mean classification error-rate of 1.7%. In contrast, pigs in TEMP before the acute heat challenge could be discriminated from the pigs in TEMP after the heat challenge with 32 OTU and 9.3% error rate. The microbiota can be used as biomarker of heat stress exposition. Microbiota composition revealed that pigs were separated into 2 enterotypes. The enterotypes were represented in both climates. Whatever the climate, animals belonging to the Turicibacter–Sarcina–Clostridium sensu stricto dominated enterotype were 3.3 kg heavier (P < 0.05) at 11 wk of age than those belonging to the Lactobacillus-dominated enterotype. This latter enterotype was related to a 0.3 °C lower skin temperature (P < 0.05) at 23 wk of age. Following the acute heat challenge in TEMP, this enterotype had a less-stable rectal temperature (0.34 vs. 0.25 °C variation between weeks 23 and 24, P < 0.05) without affecting growth performance (P > 0.05). Instability of the enterotypes was observed in 34% of the pigs, switching from an enterotype to another between 23 and 26 wk of age after heat stress. Despite a lower microbial diversity, the Turicibacter–Sarcina–Clostridium sensu stricto dominated enterotype was better adapted to heat stress conditions with lower thermoregulation variations.
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spelling pubmed-67358212019-09-16 Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,) Le Sciellour, Mathilde Zemb, Olivier Hochu, Isabelle Riquet, Juliette Gilbert, Hélène Giorgi, Mario Billon, Yvon Gourdine, Jean-Luc Renaudeau, David J Anim Sci Microbiome The present study aimed at investigating the impact of heat challenges on gut microbiota composition in growing pigs and its relationship with pigs’ performance and thermoregulation responses. From a total of 10 F1 sire families, 558 and 564 backcross Large White × Créole pigs were raised and phenotyped from 11 to 23 wk of age in temperate (TEMP) and in tropical (TROP) climates, respectively. In TEMP, all pigs were subjected to an acute heat challenge (3 wk at 29 °C) from 23 to 26 wk of age. Feces samples were collected at 23 wk of age both in TEMP and TROP climate (TEMP23 and TROP23 samples, respectively) and at 26 wk of age in TEMP climate (TEMP26 samples) for 16S rRNA analyses of fecal microbiota composition. The fecal microbiota composition significantly differed between the 3 environments. Using a generalized linear model on microbiota composition, 182 operational taxonomic units (OTU) and 2 pathways were differentially abundant between TEMP23 and TEMP26, and 1,296 OTU and 20 pathways between TEMP23 and TROP23. Using fecal samples collected at 23 wk of age, pigs raised under the 2 climates were discriminated with 36 OTU using a sparse partial least square discriminant analysis that had a mean classification error-rate of 1.7%. In contrast, pigs in TEMP before the acute heat challenge could be discriminated from the pigs in TEMP after the heat challenge with 32 OTU and 9.3% error rate. The microbiota can be used as biomarker of heat stress exposition. Microbiota composition revealed that pigs were separated into 2 enterotypes. The enterotypes were represented in both climates. Whatever the climate, animals belonging to the Turicibacter–Sarcina–Clostridium sensu stricto dominated enterotype were 3.3 kg heavier (P < 0.05) at 11 wk of age than those belonging to the Lactobacillus-dominated enterotype. This latter enterotype was related to a 0.3 °C lower skin temperature (P < 0.05) at 23 wk of age. Following the acute heat challenge in TEMP, this enterotype had a less-stable rectal temperature (0.34 vs. 0.25 °C variation between weeks 23 and 24, P < 0.05) without affecting growth performance (P > 0.05). Instability of the enterotypes was observed in 34% of the pigs, switching from an enterotype to another between 23 and 26 wk of age after heat stress. Despite a lower microbial diversity, the Turicibacter–Sarcina–Clostridium sensu stricto dominated enterotype was better adapted to heat stress conditions with lower thermoregulation variations. Oxford University Press 2019-09 2019-07-02 /pmc/articles/PMC6735821/ /pubmed/31268142 http://dx.doi.org/10.1093/jas/skz222 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Microbiome
Le Sciellour, Mathilde
Zemb, Olivier
Hochu, Isabelle
Riquet, Juliette
Gilbert, Hélène
Giorgi, Mario
Billon, Yvon
Gourdine, Jean-Luc
Renaudeau, David
Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title_full Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title_fullStr Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title_full_unstemmed Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title_short Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
title_sort effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs(,)
topic Microbiome
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6735821/
https://www.ncbi.nlm.nih.gov/pubmed/31268142
http://dx.doi.org/10.1093/jas/skz222
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