Influence of feed efficiency ranking and maternal nutrition on gut microbiome, metabolome, and transcriptome in beef and dairy cattle

Residual feed intake (RFI) describes an animal’s feed efficiency independent of the level of growth and production performance. The RFI has become a commonly used measure for feed efficiency in beef and dairy cattle. The first experiment was to determine differences in major ruminal bacteria and ruminal epithelium gene expression between most-efficient (M-eff) and least-efficient (L-eff) finishing beef cattle. Results indicated that superior feed efficiency in beef cattle is associated with differences in bacterial species and transcriptional adaptations in ruminal epithelium that might enhance nutrient delivery and utilization by tissues. For example, M-eff beef cattle enriched cellulose-degrading bacteria and volatile fatty acids (VFA) producing bacteria. Furthermore, M-eff cattle upregulated VFA absorption and ketogenesis in ruminal epithelium, underscoring greater energy production in M-eff cattle than L-eff cattle. These might have helped M-eff cattle to maintain the same level of growth performance as L-eff group while consuming less dry matter intake (DMI). The second and third experiments evaluated differences in ruminal bacteria and the activities of microbial digestive enzymes between M-eff and L-eff dairy cows during the peripartum period and early lactation. The results showed that M-eff cows enriched fibrolytic bacteria, propionate-producing bacteria, and lactate-removing bacteria whereas declined lactate-producing bacteria compared with L-eff group. The M-eff cows had lower activities for major ruminal digestive enzymes such as amylase, cellulase, xylanase, and protease than L-eff cows. These shifts in ruminal bacteria and digestive enzyme activities during the peripartum period could be a mechanism for better feed efficiency in dairy cows. The fourth experiment was to determine differences in hindgut microbiome and metabolome in neonatal dairy heifer calves retrospectively grouped as M-eff or L-eff calves during the preweaning period. Rectal swabs were collected immediately at birth before colostrum feeding (i.e., d 0), and fecal samples were collected at d 14, 28, and 42 (prior to weaning) for microbiome and untargeted metabolome analyses using 16s rRNA gene sequencing and liquid chromatography-mass spectrometry (LC-MS) approaches. Microbiome data were analyzed with QIIME 2 platform whereas metabolome data were analyzed with MetaboAnalyst 4 pipeline. Hindgut microbiome and metabolome profiles indicated that M-eff heifers had greater capacity for energy production (e.g. butyrate and propionate) and essential nutrients such as vitamins and amino acids than L-eff heifers, suggesting that M-eff heifers had extra supply of energy and nutrients. These might have helped M-eff heifers to maintain the same level of growth and development as L-eff heifers while consuming less DMI. The observed alterations in hindgut microbiome and metabolome might contribute, at least in part, to enhanced feed efficiency in neonatal dairy heifers during preweaning period. To our knowledge, most studies demonstrating the central role of manipulating maternal nutrition on hindgut microbiome in offspring have been performed with non-ruminants. Whether this phenomena exist in cattle is largely unknown. Therefore, the objective of the fifth experiment was to evaluate the impact of maternal methionine supply during late-pregnancy in dairy cows on hindgut microbiome and metabolome in neonatal calves. To achieve this, Holstein heifer calves born to cows receiving either a control (CON) diet or CON plus rumen-protected methionine (MET) during the last 28 d of pregnancy were selected for this study. Hindgut microbiome and metabolome profiles in MET heifers indicated greater capacity for the production of endogenous antibiotics and enhanced hindgut functionality and health. Those alterations could limit pathogen colonization in the hindgut while providing essential nutrients to neonatal calves. Together, such responses contribute to the ability of MET heifers to achieve better nutrient utilization to support greater growth during preweaning period compared with CON heifers without Changes in DMI