Enterosignatures of the Fecal Pig Microbiota: Exploring Determinants and Revealing Host-Performance Consequences

Abstract

Abstract The pig gut microbiota is a complex ecosystem composed of microbial guilds, which until recently were unknown. Here, we decomposed the pig fecal microbiota of 648 healthy pigs during the transition (n=400) and growing-finishing (n=248) periods in co-occurring bacterial communities defined as pig enterosignatures (pig ES). Our results indicate that fecal microbial ecosystems can accurately be described by combinations of at least six pig ES, driven by Prevotella (ES-Prev), Treponema (ES-Trep), Lactobacillus (ES-Lact), Clostridium (ES-Clost), Streptococcus (ES-Strep), and UBA2810 (ES-UBA2) genera. We observed a dynamic shift in the composition of pig ES, where ES-Prev, ES-Strep, and ES-Lact seem to be core components, while ES-Trep, ES-Clost, and ES-UBA play age-specific roles. Our results suggest partial genetic control by the host, with heritabilities of pig ES composition ranging from 0.30 to 0.42. Furthermore, our findings indicate that stress can impact pig ES assembly, decreasing ES-Lact abundance while increasing the prevalence of ES-Strep. We noted a positive link between ES-Prev and growth at 60 days, which later evolved negatively, impacting feed efficiency during the finish-growing period. Additionally, we observed a negative association of ES-Strep and a positive impact of ES-Lact on growth and feed efficiency during the growing period. Remarkably, a negative association between the abundance of ES-Lact and levels of hair cortisol was also observed during this period. Overall, our findings confirm the key ecological roles of Prevotella, Treponema, Lactobacillus, and Streptococcus from previous studies in pigs and reveal novels links with relevant porcine physiological and performance traits. Finally, despite pig ES proving valuable in dissecting microbial communities into assemblies of underlying microbial guilds, showcasing its potential as a novel tool in breeding and precision farming. Our findings emphasize the importance of customizing microbial consortia to meet the nutritional and health requirements at each stage or category of the porcine production chain.