Deterministic succession patterns in the rumen and fecal microbiome associate with host metabolic shifts in peripartum dairy cattle.

Abstract

Background: Metabolic disorders in peripartum ruminants affect health and productivity, with gut microbiota playing a key role in host metabolism. Therefore, our study aimed to characterize the gut microbiota of peripartum dairy cows to better understand the relationship between metabolic phenotypes and the rumen and fecal microbiomes during the peripartum period.

Results: In a longitudinal study of 91 peripartum cows, we analyzed rumen and fecal microbiomes via 16S rRNA and metagenomic sequencing across six time points. By using enterotype classification, ecological model, and random forest analysis, we identified distinct deterministic succession patterns in the rumen and fecal microbiomes (rumen: rapid transition-transition-stable; hindgut: stable-transition-stable). Key microbes, such as Succiniclasticum and Bifidobacterium, were found to drive microbial succession by balancing stochastic and deterministic processes. Notably, we observed that changes in gut microbiota succession patterns significantly influenced metabolic phenotypes (e.g., serum non-esterified fatty acid, glucose, and insulin levels). Mediation analysis suggested that specific gut microbes (e.g., Prevotella sp900315525 in the rumen and Alistipes sp015059845 in the hindgut) and metabolic pathways (e.g., glucose-related pathway) were associated with host metabolic phenotypes.

Conclusions: Overall, utilizing a large gut microbiome dataset and enterotype- and ecological model-based microbiome analyses, we comprehensively elucidated the succession and assembly of the gut microbiota in peripartum dairy cows. We further confirmed that changes in gut microbiota succession patterns were significantly related to the metabolic phenotypes of peripartum dairy cows. These findings provide valuable insights for developing health management strategies for peripartum ruminants.