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

Sharon A. Huws*, Joan E. Edwards, Wanchang Lin, Francesco Rubino, Mark Alston, David Swarbreck, Shabhonam Caim, Pauline Rees Stevens, Justin Pachebat, Mi-Young Won, Linda B. Oyama, Christopher J. Creevey, Alison H. Kingston-Smith

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)
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Abstract

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. CnT8ee8Emnfj-Y7oyo5rXtVideo Abstract
Original languageEnglish
Article number143
Number of pages17
JournalMicrobiome
Volume9
Issue number1
Early online date21 Jun 2021
DOIs
Publication statusPublished - Dec 2021

Bibliographical note

Funding Information:
This work was supported by the Biotechnology and Biological Sciences Research Council Institute Strategic Programme Grant, Rumen Systems Biology (grant number BBS/E/W/10964), Core Strategic Programme in Resilient Crops (BBS/E/W/0012843D) and The Genome Analysis Centre (now the Earlham Institute) Capacity and Capability Challenge Programme.

Publisher Copyright:
© 2021, The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

  • Archaea
  • Bacteria
  • Biofilm
  • Colonisation
  • Ecology
  • Metatranscriptome
  • Microbiome
  • Niche
  • Rumen
  • Temporal

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

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