Comprehensive studies illustrated that certain phenotypic characteristics could be transferred to recipients by fecal microbiota transplantation, but few have clarified the mechanism, that is, whether through the direct connection of colonized microbiota or the crosstalk via microbiota-derived metabolites. In the current study, jejunal and colonic digesta contents were collected from a slaughtered 100-day-old boar and then underwent a series of separation processes to obtain cleaned microbiota pellets (JM and CM) and pure metabolites solution (JS and CS). Sixty 23-day-old weaned piglets with similar body weights were divided into five groups and orally administered by vehicle solution (Con), JM, JS, CM, and CS, respectively, for ten days, and slaughtering on day 20. Interestingly, compared with the Con group, JM, but not JS, significantly alleviated piglet postweaning diarrhea (P<0.05) during the first week and promoted their growth, with a final BW of 0.70 kg (P=0.18) over Con group, which could be attribute to the enhanced gut development including increased stem cells' proliferation and differentiation capability and higher expressions of barrier-associated molecules E-Cadherin, MUC2+, and Villin in jejunum (P<0.05). Adult donor colonic microbiota and metabolites administrations promoted piglets’ growth at different degrees by the end of the study, with 0.75 kg (CS, P=0.10) and 0.25 kg (CM) of final BW over the Con group, respectively. Piglets gavaged with CM had promoted intestinal development, shown as increased ileal (P<0.01) and cecal unit mucosal weights (P<0.05). In addition, bacterial absolute quantification disclosed that donor’s jejunal microbiota is favored to colonize in recipients’ jejunal but not the colon, whereas colonic microbiota preferred to colonize in piglets’ colons. We further found that Megasphaera and Prevotella 9 are potentially JM and CM-derived probiotics, respectively, that colonized in piglet recipients, facilitating gut development and growth performance. Piglets fed adult CS gained promoted growth potentially by affecting their colon metabolic ecosystem through phenylalanine, tyrosine, and tryptophan biosynthesis pathways. In conclusion, direct interaction with live microbiota is a prerequisite for enhancing gut development, and adults’ colon metabolites potentially promote growth through nutritional modification.
Keywords: microbiome transplantation, colonization, metabolome, intestinal barrier, stem cells