BackgroundResidual feed intake (RFI) describes an animal’s feed efficiency independent of growth performance. The objective of this study was to determine differences in growth performance, carcass traits, major bacteria attached to ruminal solids-fraction, and ruminal epithelium gene expression between the most-efficient and the least-efficient beef cattle. One-hundred and forty-nine Red Angus cattle were allocated to three contemporary groups according to sex and herd origin. Animals were fed a finishing diet in confinement for 70 d to determine the RFI category for each. Within each group, the two most-efficient (n = 6; RFI coefficient = − 2.69 ± 0.58 kg dry matter intake (DMI)/d) and the two least-efficient animals (n = 6; RFI coefficient = 3.08 ± 0.55 kg DMI/d) were selected. Immediately after slaughter, ruminal solids-fraction and ruminal epithelium were collected for bacteria relative abundance and epithelial gene expression analyses, respectively, using real-time PCR.ResultsThe most-efficient animals consumed less feed (P = 0.01; 5.03 kg less DMI/d) compared with the least-efficient animals. No differences (P > 0.10) in initial body weight (BW), final BW, and average daily gain (ADG) were observed between the two RFI classes. There were no significant RFI × sex effects (P > 0.10) on growth performance. Compared with the least-efficient group, hot carcass weight (HCW), ribeye area (REA), and kidney, pelvic, and heart fat (KPH) were greater (P ≤ 0.05) in the most-efficient cattle. No RFI × sex effect (P > 0.10) for carcass traits was detected between RFI groups. Of the 10 bacterial species evaluated, the most-efficient compared with least efficient cattle had greater (P ≤ 0.05) relative abundance of Eubacterium ruminantium, Fibrobacter succinogenes, and Megasphaera elsdenii, and lower (P ≤ 0.05) Succinimonas amylolytica and total bacterial density. No RFI × sex effect on ruminal bacteria was detected between RFI groups. Of the 34 genes evaluated in ruminal epithelium, the most-efficient cattle had greater (P ≤ 0.05) abundance of genes involved in VFA absorption, metabolism, ketogenesis, and immune/inflammation-response. The RFI × sex interactions indicated that responses in gene expression between RFI groups were due to differences in sex. Steers in the most-efficient compared with least-efficient group had greater (P ≤ 0.05) expression of SLC9A1, HIF1A, and ACO2. The most-efficient compared with least-efficient heifers had greater (P ≤ 0.05) mRNA expression of BDH1 and lower expression (P ≤ 0.05) of SLC9A2 and PDHA1.ConclusionsThe present study revealed that greater feed efficiency in beef cattle is associated with differences in bacterial species and transcriptional adaptations in the ruminal epithelium that might enhance nutrient delivery and utilization by tissues. The lack of RFI × sex interaction for growth performance and carcass traits indicates that sex may not play a major role in improving these phenotypes in superior RFI beef cattle. However, it is important to note that this result should not b...