The impact of wild-boar derived microbiota transplantation on piglet microbiota, metabolite profile and gut proinflammatory cytokine production differs from sow-derived microbiota

Colonization of co-evolved, species-specific microbes in early life plays a crucial role in gastrointestinal development and immune function. This study hypothesized modern pig production practices have resulted in the loss of co-evolved species and critical symbiotic host- microbe interactions. To test this, we reintroduced microbes from wild boars (WB) into conventional piglets to explore their colonization dynamics and effects on gut microbial communities, metabolite profiles, and immune responses. At postnatal day (PND) 21, 48 piglets were assigned to four treatment groups: 1) WB-derived mixed microbial community (MMC), 2) sow-derived MMC, 3) a combination of WB and sow MMC (Mix), or 4) Control (PBS). Post- transplantation analyses at PND 48 revealed distinct microbial communities in WB-inoculated piglets compared to Controls, with trends toward differentiation from Sow but not Mix groups. WB-derived microbes were more successful in colonizing piglets, particularly in the Mix group, where they competed with sow-derived microbes. WB group cecal digesta enriched with Lactobacillus helveticus, Lactobacillus mucosae, and Lactobacillus pontis. Cecal metabolite analysis showed that WB piglets were enriched in histamine, acetyl-ornithine, ornithine, citrulline, and other metabolites, with higher histamine levels linked to Lactobacillus abundance. WB piglets exhibited lower cecal IL-1{beta} and IL-6 levels compared to Controls and Sow groups, while the Mix group showed reduced IFN-{gamma}, IL-2, and IL-6 compared to the Sow group. No differences in weight gain, fecal scores, or plasma cytokines were observed, indicating no adverse effects. These findings support that missing WB microbes effectively colonize domestic piglets and may positively impact metabolite production and immune responses. ImportanceThis study addresses the growing concern over losing co-evolved, species-specific microbes in modern agricultural practices, particularly in pig production. The implementation of strict biosecurity measures and widespread antibiotic use in conventional farming systems may disrupt crucial host-microbe interactions that are essential for gastrointestinal development and immune function. Our research demonstrates that by reintroducing wild boar-derived microbes into domestic piglets, these co-evolved microbes can successfully colonize the gut, influence microbial community composition, and alter metabolite profiles and immune responses without causing adverse effects. These findings also suggest that these co-evolved microbes can fill an intestinal niche, positively impacting immune activation. This research lays the groundwork for future strategies to enhance livestock health and performance by restoring natural microbial populations that produce immune-modulating metabolites. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=156 SRC="FIGDIR/small/623678v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@6ec5c2org.highwire.dtl.DTLVardef@79804corg.highwire.dtl.DTLVardef@d63016org.highwire.dtl.DTLVardef@1ef0010_HPS_FORMAT_FIGEXP M_FIG C_FIG