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Background  Gut microbiomes, such as the rumen, greatly influence host nutrition due to their feed energy-harvesting capacity. We investigated temporal ecological interactions facilitating energy harvesting at the fresh perennial ryegrass (PRG)-biofilm interface in the rumen using an in sacco approach and prokaryotic metatranscriptomic profiling.    Results  Network analysis identified two distinct sub-microbiomes primarily representing primary (≤ 4 h) and secondary (≥ 4 h) colonisation phases and the most transcriptionally active bacterial families (i.e  Fibrobacteriaceae ,  Selemondaceae  and  Methanobacteriaceae ) did not interact with either sub-microbiome, indicating non-cooperative behaviour. Conversely,  Prevotellaceae  had most transcriptional activity within the primary sub-microbiome (focussed on protein metabolism) and  Lachnospiraceae  within the secondary sub-microbiome (focussed on carbohydrate degradation). Putative keystone taxa, with low transcriptional activity, were identified within both sub-microbiomes, highlighting the important synergistic role of minor bacterial families; however, we hypothesise that they may be ‘cheating’ in order to capitalise on the energy-harvesting capacity of other microbes. In terms of chemical cues underlying transition from primary to secondary colonisation phases, we suggest that AI-2-based quorum sensing plays a role, based on LuxS gene expression data, coupled with changes in PRG chemistry.    Conclusions  In summary, we show that fresh PRG-attached prokaryotes are resilient and adapt quickly to changing niches. This study provides the first major insight into the complex temporal ecological interactions occurring at the plant-biofilm interface within the rumen. The study also provides valuable insights into potential plant breeding strategies for development of the utopian plant, allowing optimal sustainable production of ruminants.Video AbstractSupplementary Information  The online version contains supplementary material available at 10.1186/s40168-021-01087-w.

Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches