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Selection for environmental variance shifted the gut microbiome composition driving animal resilience

BACKGROUND: Understanding how the host’s microbiome shapes phenotypes and participates in the host response to selection is fundamental for evolutionists and animal and plant breeders. Currently, selection for resilience is considered a critical step in improving the sustainability of livestock syst...

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Autores principales: Casto-Rebollo, Cristina, Argente, María José, García, María Luz, Pena, Ramona Natacha, Blasco, Agustín, Ibáñez-Escriche, Noelia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10318751/
https://www.ncbi.nlm.nih.gov/pubmed/37400907
http://dx.doi.org/10.1186/s40168-023-01580-4
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author Casto-Rebollo, Cristina
Argente, María José
García, María Luz
Pena, Ramona Natacha
Blasco, Agustín
Ibáñez-Escriche, Noelia
author_facet Casto-Rebollo, Cristina
Argente, María José
García, María Luz
Pena, Ramona Natacha
Blasco, Agustín
Ibáñez-Escriche, Noelia
author_sort Casto-Rebollo, Cristina
collection PubMed
description BACKGROUND: Understanding how the host’s microbiome shapes phenotypes and participates in the host response to selection is fundamental for evolutionists and animal and plant breeders. Currently, selection for resilience is considered a critical step in improving the sustainability of livestock systems. Environmental variance (V (E)), the within-individual variance of a trait, has been successfully used as a proxy for animal resilience. Selection for reduced V (E) could effectively shift gut microbiome composition; reshape the inflammatory response, triglyceride, and cholesterol levels; and drive animal resilience. This study aimed to determine the gut microbiome composition underlying the V (E) of litter size (LS), for which we performed a metagenomic analysis in two rabbit populations divergently selected for low (n = 36) and high (n = 34) V (E) of LS. Partial least square-discriminant analysis and alpha- and beta-diversity were computed to determine the differences in gut microbiome composition among the rabbit populations. RESULTS: We identified 116 KEGG IDs, 164 COG IDs, and 32 species with differences in abundance between the two rabbit populations studied. These variables achieved a classification performance of the V (E) rabbit populations of over than 80%. Compared to the high V (E) population, the low V (E) (resilient) population was characterized by an underrepresentation of Megasphaera sp., Acetatifactor muris, Bacteroidetes rodentium, Ruminococcus bromii, Bacteroidetes togonis, and Eggerthella sp. and greater abundances of Alistipes shahii, Alistipes putredinis, Odoribacter splanchnicus, Limosilactobacillus fermentum, and Sutterella, among others. Differences in abundance were also found in pathways related to biofilm formation, quorum sensing, glutamate, and amino acid aromatic metabolism. All these results suggest differences in gut immunity modulation, closely related to resilience. CONCLUSIONS: This is the first study to show that selection for V (E) of LS can shift the gut microbiome composition. The results revealed differences in microbiome composition related to gut immunity modulation, which could contribute to the differences in resilience among rabbit populations. The selection-driven shifts in gut microbiome composition should make a substantial contribution to the remarkable genetic response observed in the V (E) rabbit populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01580-4.
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spelling pubmed-103187512023-07-05 Selection for environmental variance shifted the gut microbiome composition driving animal resilience Casto-Rebollo, Cristina Argente, María José García, María Luz Pena, Ramona Natacha Blasco, Agustín Ibáñez-Escriche, Noelia Microbiome Research BACKGROUND: Understanding how the host’s microbiome shapes phenotypes and participates in the host response to selection is fundamental for evolutionists and animal and plant breeders. Currently, selection for resilience is considered a critical step in improving the sustainability of livestock systems. Environmental variance (V (E)), the within-individual variance of a trait, has been successfully used as a proxy for animal resilience. Selection for reduced V (E) could effectively shift gut microbiome composition; reshape the inflammatory response, triglyceride, and cholesterol levels; and drive animal resilience. This study aimed to determine the gut microbiome composition underlying the V (E) of litter size (LS), for which we performed a metagenomic analysis in two rabbit populations divergently selected for low (n = 36) and high (n = 34) V (E) of LS. Partial least square-discriminant analysis and alpha- and beta-diversity were computed to determine the differences in gut microbiome composition among the rabbit populations. RESULTS: We identified 116 KEGG IDs, 164 COG IDs, and 32 species with differences in abundance between the two rabbit populations studied. These variables achieved a classification performance of the V (E) rabbit populations of over than 80%. Compared to the high V (E) population, the low V (E) (resilient) population was characterized by an underrepresentation of Megasphaera sp., Acetatifactor muris, Bacteroidetes rodentium, Ruminococcus bromii, Bacteroidetes togonis, and Eggerthella sp. and greater abundances of Alistipes shahii, Alistipes putredinis, Odoribacter splanchnicus, Limosilactobacillus fermentum, and Sutterella, among others. Differences in abundance were also found in pathways related to biofilm formation, quorum sensing, glutamate, and amino acid aromatic metabolism. All these results suggest differences in gut immunity modulation, closely related to resilience. CONCLUSIONS: This is the first study to show that selection for V (E) of LS can shift the gut microbiome composition. The results revealed differences in microbiome composition related to gut immunity modulation, which could contribute to the differences in resilience among rabbit populations. The selection-driven shifts in gut microbiome composition should make a substantial contribution to the remarkable genetic response observed in the V (E) rabbit populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01580-4. BioMed Central 2023-07-04 /pmc/articles/PMC10318751/ /pubmed/37400907 http://dx.doi.org/10.1186/s40168-023-01580-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Casto-Rebollo, Cristina
Argente, María José
García, María Luz
Pena, Ramona Natacha
Blasco, Agustín
Ibáñez-Escriche, Noelia
Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title_full Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title_fullStr Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title_full_unstemmed Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title_short Selection for environmental variance shifted the gut microbiome composition driving animal resilience
title_sort selection for environmental variance shifted the gut microbiome composition driving animal resilience
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10318751/
https://www.ncbi.nlm.nih.gov/pubmed/37400907
http://dx.doi.org/10.1186/s40168-023-01580-4
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