Multi-omics profiling of sow colostrum and faecal microbiota reveals parity-dependent and independent factors associated with piglet survival and growth

Background Colostrum is recognised as the “golden elixir of health” due to its optimal chemical, immunological and nutraceutical properties for newborns, but little is known about its nature in the pig. This study aims to provide a multi-omics characterisation of pig colostrum from different parities (gilts, n = 7, second, n = 7 and mature, n = 6 sows) to identify the most relevant bioactive compounds associated with piglet survival and average daily gain (ADG) and faecal microbiota till d 6 and d 24. Results Nine hundred and fifty metabolites (108 chemically confirmed) and 71 fatty acids (FAs) were characterised in colostrum. Parity class was the main driver for piglet survivability (P < 0.001; highest in second parity), metabolomics (R2 = 0.97; Q2 = 0.52; > 200 discriminated metabolites) and lipidomic profile (22 discriminated FAs) and piglet faecal microbiota (beta diversity P < 0.05 at d 6 and d 24). Colostrum composition allowed clustering for piglet mortality from d 0 to d 6 (Q2 > 0.50). Mortality classes at d 6 were discriminated by 177 metabolites and 2 FAs and 248 metabolites and 21 FAs at d 24. At both timepoints a higher abundance of C18:2 8trans,10cis discriminated for lower mortality (importance = 1 for d 6 and 0.34 for d 24). Pathway analysis at d 6 and d 24 indicated arginine biosynthesis and alpha-linoleic acid metabolism as most enriched metabolism in swine colostrum related to higher survivability. The multi-omics integration analysis revealed that a higher faecal abundance of Lachnospiraceae_FCS020, Holdemania, Roseburia, and a higher colostrum abundance of C18:2 8trans,10cis, and the C18:1 5trans and salicylic acid as metabolites were the most associated with a lower mortality. The ADG classes d 0–24 were discriminated by 151 metabolites and 33 FAs. Higher ADG (240 g/d) was discriminated by colostrum vitamin E, histidine, and branched-chain amino acids (VIP score > 1), while L-kynurenine and gamma-aminobutyric acid were linked to lower growth, suggesting maternal stress. Conclusion This study confirms the importance of parity order in shaping colostrum composition and identifies several bioactive compounds, some parity-dependent and others parity-independent, that may be associated with improved piglet survival and gut microbiota maturation. The findings may also support the development of next-generation artificial colostrum supplements.