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

Abstract 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 livest...

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Main Authors: Cristina Casto-Rebollo, María José Argente, María Luz García, Ramona Natacha Pena, Agustín Blasco, Noelia Ibáñez-Escriche
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Microbiome
Online Access:https://doi.org/10.1186/s40168-023-01580-4
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author Cristina Casto-Rebollo
María José Argente
María Luz García
Ramona Natacha Pena
Agustín Blasco
Noelia Ibáñez-Escriche
author_facet Cristina Casto-Rebollo
María José Argente
María Luz García
Ramona Natacha Pena
Agustín Blasco
Noelia Ibáñez-Escriche
author_sort Cristina Casto-Rebollo
collection DOAJ
description Abstract 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. Video Abstract
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spelling doaj.art-72b7fd4ea08b43739e44dcff6185da132023-07-09T11:19:32ZengBMCMicrobiome2049-26182023-07-011111910.1186/s40168-023-01580-4Selection for environmental variance shifted the gut microbiome composition driving animal resilienceCristina Casto-Rebollo0María José Argente1María Luz García2Ramona Natacha Pena3Agustín Blasco4Noelia Ibáñez-Escriche5Institute for Animal Science and Technology, Universitat Politècnica de ValènciaCentro de Investigación e Innovación Agroalimentaria Y Agroambiental (CIAGRO_UMH), Miguel Hernández UniversityCentro de Investigación e Innovación Agroalimentaria Y Agroambiental (CIAGRO_UMH), Miguel Hernández UniversityDepartament de Ciència Animal, Universitat de Lleida-AGROTECNIO CenterInstitute for Animal Science and Technology, Universitat Politècnica de ValènciaInstitute for Animal Science and Technology, Universitat Politècnica de ValènciaAbstract 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. Video Abstracthttps://doi.org/10.1186/s40168-023-01580-4
spellingShingle Cristina Casto-Rebollo
María José Argente
María Luz García
Ramona Natacha Pena
Agustín Blasco
Noelia Ibáñez-Escriche
Selection for environmental variance shifted the gut microbiome composition driving animal resilience
Microbiome
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
url https://doi.org/10.1186/s40168-023-01580-4
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