The impact of early-life rearing conditions on the porcine gut microbiota and immune system.
Luke Comer, Muhammad Zeeshan Akram, Haoran Zhao, Peiyang Huo, Ester Arévalo Sureda, Chuanpi Xiao, Hikmat Ullah Khan Usman, Pawel Siegien, José Wavreille, Jan Aerts, Nadia Everaert
Abstract
Open AccessBACKGROUND: Early life represents an unparalleled window in the life of the pig in which the gut microbiota interacts with its host's naïve immune system. Yet, modern swine production often favours conditions that promote production efficiency rather than enriched microbiota development, the long-term consequences of which remain poorly understood. This study sought to analyse the long-term impacts of early-life rearing conditions on the gut microbiota until day 90, and in turn, its physiological and immunological consequences. We established two rearing conditions from farrowing until day 90: enriched, microbiota-enhancing husbandry characterised by weaning at 6 weeks and the provision of litter material throughout; and restricted, microbiota-depleting husbandry comprising weaning at 3 weeks and antibiotic administration from days 2 to 9. The day 42 faecal, and day 90 ileal and faecal microbiotas underwent 16 S V1-V9 rRNA gene sequencing. Intestinal and faecal volatile fatty acids were measured via gas chromatography, haematological parameters were assessed from whole blood, and serum immunoglobulin G was measured. Immune-focused gene expression in the spleen and ileum was also measured via qPCR. RESULTS: The faecal microbiota exhibited differential β-diversity by group at both timepoints. On day 90, enriched pigs exhibited significantly elevated ileal villus height to crypt depth ratios, which were negatively correlated with serum IgG. Conversely, restricted pigs had more branched-chain fatty acids in the colon and faeces, alongside signs of heightened immune activity, with haematology showing enhanced neutrophil activation, and elevated lymphocyte and IgG levels. In the spleen, gene sets comprising genes for the pro-inflammatory cytokines IL-6, IL-15 and IFN-γ were upregulated among restricted pigs, while enriched pigs exhibited better-primed innate immune systems. CONCLUSIONS: These findings demonstrate long-term impacts of early-life rearing on faecal microbiota composition. We furthermore observed a potential shift towards inflammation and altered haematology associated with the microbiota.