Effect of environmental variance-based resilience selection on the gut metabolome of rabbits

Abstract

Background Gut metabolites are key actors in host-microbiota crosstalk with effect on health. The study of the gut metabolome is an emerging topic in livestock, which can help understand its effect on key traits such as animal resilience and welfare. Animal resilience has now become a major trait of interest because of the high demand for more sustainable production. Composition of the gut microbiome can reveal mechanisms that underlie animal resilience because of its influence on host immunity. Environmental variance (VE), specifically the residual variance, is one measure of resilience. The aim of this study was to identify gut metabolites that underlie differences in the resilience potential of animals originating from a divergent selection for VE of litter size (LS). We performed an untargeted gut metabolome analysis in two divergent rabbit populations for low (n = 13) and high (n = 13) VE of LS. Partial least square-discriminant analysis was undertaken, and Bayesian statistics were computed to determine dissimilarities in the gut metabolites between these two rabbit populations. Results We identified 15 metabolites that discriminate rabbits from the divergent populations with a prediction performance of 99.2% and 90.4% for the resilient and non-resilient populations, respectively. These metabolites were suggested to be biomarkers of animal resilience as they were the most reliable. Among these, five that derived from the microbiota metabolism (3-(4-hydroxyphenyl)lactate, 5-aminovalerate, and equol, N6-acetyllysine, and serine), were suggested to be indicators of dissimilarities in the microbiome composition between the rabbit populations. The abundances of acylcarnitines and metabolites derived from the phenylalanine, tyrosine, and tryptophan metabolism were low in the resilient population and these pathways can, therefore impact the inflammatory response and health status of animals. Conclusions This is the first study to identify gut metabolites that could act as potential resilience biomarkers. The results support differences in resilience between the two studied rabbit populations that were generated by selection for VE of LS. Furthermore, selection for VE of LS modified the gut metabolome, which could be another factor that modulates animal resilience. Further studies are needed to determine the causal role of these metabolites in health and disease.

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

“…2 ). The latter supported the differences found in the gut metabolite formiminoglutamate, which was found to be lower in the rabbits from the low VE population [ 40 ]. Differences in glutamate levels were also observed [ 40 ].…”

“…2 ). A gut metabolomic study suggested differences in the feed efficiency between these rabbit populations [ 40 ] which could explain the differences in the abundance of Ruminococcus bromii . Ruminococcus bromii is a keystone in breaking down starch, allowing other gut microbiota species to cross-feed [ 41 ].…”

A first characterization of the Microbiota-Resilience Link in Swine

“…However, a noteworthy study by Blasco et al in 2017, which focused on divergent selection for variability in rabbit litter size, challenges this notion. Subsequent investigations on this particular population, employing genomic analysis [18] and metabolic pro ling [20], unveiled a link between this variability and a more comprehensive notion of animal resilience. These ndings align with later studies that also observed associations between genomic pro les and resilience, even in the absence of intentional stress induction, as in our current study [16,38].…”

“…Consequently, recent investigations have prioritized unraveling the association between the microbiome and resilience. Studies have examined resilience in various contexts, encompassing the resistance of coral to climate changes [44,45], the practical implications of microbiome engineering in plants [20], and the role of microbial composition in thermal stress adaptations across different animal species, including tadpoles [46], Drosophila [47], and mice [48]. However, within the domain of livestock, only one study conducted by Casto-Rebollo et al in 2023 in rabbits has explored the relationship between the microbiome and resilience [21].…”

“…This approach may overlook important intermediate layers that exist between resilience and the host or animal's physiology. Recent studies [20,21] highlights one such intermediate layer by demonstrating the value of new omics approaches, particularly gut metabolomics and microbiome, in identifying novel factors, such as the in ammatory response, that are linked to the animal's resilience. In fact, research on the host-microbiota relationship has emerged as a valuable tool in elucidating eco-evolutionary processes, including resilience and its phenotypic expression [22].…”