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. Video Abstract.
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Claims 7
Claim · model-written summary
Network analysis identified two distinct sub-microbiomes of perennial ryegrass-attached prokaryotes, representing primary and secondary colonisation phases.
- Taxon
- perennial ryegrass
Lolium perennee0 - Outcome
- two distinct sub-microbiomese1
- Qualifier
- primary (≤ 4 h) and secondary (≥ 4 h) colonisation phasese1
- Setting
- in the rumene0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e1“Network analysis identified two distinct sub-microbiomes primarily representing primary (≤ 4 h) and secondary (≥ 4 h) colonisation phases”
Claim · model-written summary
Prevotellaceae had the most transcriptional activity within the primary sub-microbiome, focused on protein metabolism.
- Taxon
- perennial ryegrassLolium perennee0
- Interactor
- PrevotellaceaePrevotellaceaee2other
- Outcome
- transcriptional activitye2
- Direction
- moste2
- Qualifier
- focussed on protein metabolisme2
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e2“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)”
Claim · model-written summary
Lachnospiraceae had the most transcriptional activity within the secondary sub-microbiome, focused on carbohydrate degradation.
- Taxon
- perennial ryegrassLolium perennee0
- Interactor
- LachnospiraceaeLachnospiraceaee2other
- Outcome
- transcriptional activitye2
- Direction
- moste2
- Qualifier
- focussed on carbohydrate degradatione2
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e2“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)”
Claim · model-written summary
Putative keystone taxa with low transcriptional activity were identified within both sub-microbiomes, pointing to a synergistic role of minor bacterial families.
- Taxon
- perennial ryegrassLolium perennee0
- Outcome
- Putative keystone taxae3
- Qualifier
- with low transcriptional activitye3
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e3“Putative keystone taxa, with low transcriptional activity, were identified within both sub-microbiomes, highlighting the important synergistic role of minor bacterial families”
Claim · model-written summary
The most transcriptionally active bacterial families did not interact with either sub-microbiome, indicating non-cooperative behaviour.
- Taxon
- perennial ryegrassLolium perennee0
- Interactor
- Fibrobacteriaceae, Selemondaceae and Methanobacteriaceaee4other
- Outcome
- did not interact with either sub-microbiomee4
- Qualifier
- non-cooperative behavioure4
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e4“the most transcriptionally active bacterial families (i.e Fibrobacteriaceae, Selemondaceae and Methanobacteriaceae) did not interact with either sub-microbiome, indicating non-cooperative behaviour”
Claim · model-written summary
AI-2-based quorum sensing is suggested to drive the transition from primary to secondary colonisation phases, based on LuxS gene expression and changes in perennial ryegrass chemistry.
- Taxon
- perennial ryegrassLolium perennee0
- Gene
- LuxSe5
- Compound
- AI-2e5
- Outcome
- transition from primary to secondary colonisation phasese5
- Qualifier
- changes in PRG chemistrye5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e5“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”
Claim · model-written summary
Fresh perennial ryegrass-attached prokaryotes are resilient and adapt quickly to changing niches.
- Taxon
- perennial ryegrassLolium perennee0
- Outcome
- resilient and adapt quickly to changing nichese6
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“fresh perennial ryegrass (PRG)-biofilm interface in the rumen”
e6“we show that fresh PRG-attached prokaryotes are resilient and adapt quickly to changing niches”