Sex-induced alterations in rumen microbial communities and metabolite profiles: implications for lamb body weight.

Abstract

Background: Microbiota-metabolome interactions play a crucial role in host physiological regulation and metabolic homeostasis. The aim of this study was to investigate that sex induces alterations in rumen microbial community composition and metabolite profiles in lambs and the influence on body weight. This study aimed to demonstrate that sex- induced alterations in rumen microbial community and metabolite profiles and blood indices and their linkage to growth performance in lambs.

Results: This study examined (growth indices, serum indices, rumen fermentation parameters, rumen fluid microbiota community and metabolome profiles) in 180 Hu lambs (90 males, and 90 females) with the same age and diet. At six months, male lambs showed significantly greater body weight, serum indices (glutamic pyruvic transaminase, glutamic oxalacetic transaminase, growth hormone, glucagon-like peptide 1, and ghrelin), and molar percentage of propionic acid, isobutyric acid, butyric acid, isovaleric acid and valeric acid compared to female. However, male had lower VFA molar concentrations (acetic acid, propionic acid, butyric acid, and TVFAs), acetic acid/propionic acid, and VFA molar percentage (acetic acid) than female. Significant sex-related differences were observed in rumen microbiota and metabolic enrichment between genders. Moreover, compared with the females lambs, the relative abundance of Succiniclasticum, uncultured_rumen_bacterium, NK4 A214_group, Veillonellaceae_UCG_001 and Butyrivibrio in the male lambs has been significantly increased, while the relative abundance of Prevotella has been significantly decreased (P < 0.05). Notably, there were significant rumen microbiota-metabolite interactions, especially Firmicutes and Bacteroidota as dominant phyla in the sheep rumen with significant differences in correlation with rumen metabolic modules. Additionally, there are pronounced correlations among the microbiota, particularly within the Firmicutes phylum. Furthermore, the up-regulated metabolites in the rumen fluid of male lambs were predominantly enriched in the amino acid metabolite pathway, and these metabolites exhibited a significant positive correlation with body weight. However, the metabolites that were up-regulated in ewe lambs were predominantly enriched in the lipid metabolic pathway, and these metabolites exhibited a significant negative correlation with body weight. Moreover, lamb rumen microbial markers (Lachnospiraceae_UCG_008, Saccharofermentans, unclassified_Clostridia, Christensenellaceae_R_7_group, Anaerovorax, Mogibacterium, and unclassified_Erysipelotrichaceae) and metabolic markers (C75, 4-Coumarate, Flibanserin,3-Amino-5-mercapto-1,2,4-triazole, 1,3-Propane sultone, Fingolimod phosphate ester, S-,) were significantly positively correlated with body weight, but lamb rumen microbial markers (Anaeroplasma, unclassified_Acholeplasmataceae, uncultured_rumen_bacterum_4c28 d_15) and metabolic markers (Mozenavir, Reduced riboflavin, PG(18:2(9Z,12Z)/0:0), Cowanin) were significantly negatively correlated body weight.

Conclusions: This study shows that sex-induced alterations in rumen microbial communities and metabolite profiles, adapting to the growth and development of lambs. The findings may help develop targeted strategies to optimize sheep rumen microbiota and improve productivity.