Microbiome network traits in the rumen predict average daily gain in beef cattle under different backgrounding systems

BACKGROUND: Backgrounding (BKG), the stage between weaning and finishing, significantly impacts feedlot performance in beef cattle; however, the contributions of the rumen microbiome to this growth stage remain unexplored. A longitudinal study was designed to assess how BKG affects rumen bacterial communities and average daily gain (ADG) in beef cattle. At weaning, 38 calves were randomly assigned to three BKG systems for 55 days (d): a high roughage diet within a dry lot (DL, n = 13); annual cover crop within a strip plot (CC, n = 13); and perennial pasture vegetation within rotational paddocks (PP, n = 12), as before weaning. After BKG, all calves were placed in a feedlot for 142 d and finished with a high energy ration. Calves were weighed periodically from weaning to finishing to determine ADG. Rumen bacterial communities were profiled by collecting fluid samples via oral probe and sequencing the V4 region of the 16S rRNA bacterial gene, at weaning, during BKG and finishing. RESULTS: Rumen bacterial communities diverged drastically among calves once they were placed in each BKG system, including sharp decreases in alpha diversity for CC and DL calves only (P < 0.001). During BKG, DL calves showed a substantial increase of Proteobacteria (Succinivibrionaceae family) (P < 0.001), which also corresponded with greater ADG (P < 0.05). At the finishing stage, Proteobacteria bloomed for all calves, with no previous alpha or beta diversity differences being retained between groups. However, at finishing, PP calves showed a compensatory ADG, particularly greater than that in calves coming from DL BKG (P = 0.02). Microbiome network traits such as lower average shortest path length, and increased neighbor connectivity, degree, number and strength of bacterial interactions between rumen bacteria better predicted ADG during BKG and finishing than variation in specific taxonomic profiles. CONCLUSIONS: Bacterial co-abundance interactions, as measured by network theory approaches, better predicted growth performance in beef cattle during BKG and finishing, than the abundance of specific taxa. These findings underscore the importance of early post weaning stages as potential targets for feeding interventions that can enhance metabolic interactions between rumen bacteria, to increase productive performance in beef cattle. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00175-y.