Background: Methane emissions from ruminants contribute to global warming and lead to energy loss from the ingested feed. Reducing methane emissions while increasing feed efficiency is one of the most important challenges facing the livestock industry. Previous studies have reported differences in lactate-metabolizing bacteria in the rumen between low-methane yield (LMY) and high-methane yield (HMY) sheep. It was hypothesized that methane emissions might also be related to the growth of certain bacteria. The objective of this study was to investigate the correlation between the growth and metabolism of rumen bacteria and methane emissions in sheep.Results: The growth rates of 21 species-level and 12 genera-level rumen bacterial populations were predicted based on the peak-to-trough ratio of their metagenomic sequences that were generated from two groups of sheep differing in methane yield (LMY vs. HMY). The growth rate of Faecalibacterium prausnitzii was found to be significantly different between the LMY sheep and the HMY sheep. The relative abundance of F. prausnitzii was significantly lower in the LMY sheep than the HMY sheep, whereas the relative abundance of Intestinibaculum porci and Megasphaera elsdenii was significantly higher in the LMY sheep than the HMY sheep. Metatranscriptomic analysis showed that in the LMY sheep the expression of energy-related genes of F. prausnitzii, including those involved in butyrate production, was significantly upregulated compared to the HMY sheep. Conclusions: The current study revealed a negative association between the growth rate of F. prausnitzii in the rumen and methane yield in sheep and between the growth rate of F. prausnitzii and the expression of its genes involved in energy metabolism including butyrate production. Our result also showed enrichment of lactate-producing bacteria (i.e., I. porci) and lactate-utilizing bacteria (i.e., M. elsdenii) in the LMY sheep. Together with the reported metabolic response of F. prausnitzii to lactic acid bacteria, our study corroborates the association between lactate-metabolizing bacteria and methane emissions via promoting butyrate production. M. elsdenii, I. porci, and F. prausnitzii may serve as biomarkers of methane yield from sheep, and possibly other ruminants.