COS 56-2 - Domestication affects the functional response of pig gut microbiomes against pathogens

Abstract: Domestication has shaped the gut microbiome of animals, with microbes responding to novel host traits and environments produced by human intervention. This domestic gut microbiome may contribute to host phenotypes that are adaptive for domestication and may even been under selection. We hypothesized the domestic gut microbiome, compared to the wild one, may protect against infection in contemporary agricultural settings where animals live in high density, are exposed to novel microbes, and experience high pathogen pressure. Alternatively, disturbances to the gut microbiome because of domestication may reduce microbiome-mediated colonization resistance and contribute to elevated pathogen levels.

We investigated how domestication affected the pig gut microbiome and its functional response to pathogens from a range of domestic and wild populations under diverse ecological conditions (i.e., domestication contexts). Pigs across these domestication contexts experience varying environments, diets, and degrees of antibiotic use. We characterized gut microbiome composition and gene content using amplicon and shotgun metagenomic sequencing and quantified the abundance of potentially zoonotic bacterial pathogens. We utilized in vitro cultivation experiments to test for differences in microbially-mediated colonization resistance between wild and domestic pigs. We measured colonization resistance by inoculating gut microbial communities with Salmonella enterica and deemed communities resistant if S. enterica either failed to colonize or if abundances were lower than inoculation level. We also tested if antibiotic treatment mediates colonization resistance.

Domestication context was a significant predictor of microbial composition (PERMANOVA, F-statistic=17.99, R²=0.24, p< 0.001) and functional potential (F-statistic=5.44, R²=0.21, p< 0.001). Domestic pigs harbored higher abundances of potential bacterial pathogen compared to wild pigs (Wilcoxon rank sum test, p< 0.001). Our in vitro experiments illuminate a potential mechanism for this pattern, as gut microbiomes of domestic pigs displayed lower colonization resistance compared to those of wild pigs (Wilcoxon rank sum test, p=0.007). Interestingly, subtherapeutic antibiotic treatment lowered colonization resistance for gut microbiomes of wild pigs (Wilcoxon rank sum test, p< 0.001), but microbiomes of domestic pigs were unaffected. Our findings suggest that gut microbiome changes associated with domestication have functional implications that are potentially costly. Antibiotic effects in domestic pig microbiomes may already be entrained such that dosing communities with more antibiotics does not drastically impact colonization resistance. However, because wild pig microbiomes displayed lower resistance when treated with antibiotics, this suggests that antibiotics in fact may play a role, alongside other factors, in low resistance in domestic pigs.