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

doi:10.1186/s40168-021-01087-w

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

School of Biological Sciences

Research output: Contribution to journal › Article › peer-review

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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 language	English
Article number	143
Number of pages	17
Journal	Microbiome
Volume	9
Issue number	1
Early online date	21 Jun 2021
DOIs	https://doi.org/10.1186/s40168-021-01087-w https://doi.org/10.1186/s40168-021-01087-w
Publication status	Published - 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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Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches
Copyright 2021 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
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Huws, S. A., Edwards, J. E., Lin, W., Rubino, F., Alston, M., Swarbreck, D., Caim, S., Stevens, P. R., Pachebat, J., Won, M.-Y., Oyama, L. B., Creevey, C. J., & Kingston-Smith, A. H. (2021). Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches. Microbiome, 9(1), Article 143. https://doi.org/10.1186/s40168-021-01087-w, https://doi.org/10.1186/s40168-021-01087-w

@article{dec78407304549b4993e63c5c8668e93,

title = "Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches",

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 {\textquoteleft}cheating{\textquoteright} 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",

keywords = "Archaea, Bacteria, Biofilm, Colonisation, Ecology, Metatranscriptome, Microbiome, Niche, Rumen, Temporal",

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

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: {\textcopyright} 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = dec,

doi = "10.1186/s40168-021-01087-w",

language = "English",

volume = "9",

journal = "Microbiome",

issn = "2049-2618",

publisher = "BioMed Central Ltd",

number = "1",

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Huws, SA, Edwards, JE, Lin, W, Rubino, F, Alston, M, Swarbreck, D, Caim, S, Stevens, PR, Pachebat, J, Won, M-Y, Oyama, LB , Creevey, CJ & Kingston-Smith, AH 2021, 'Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches', Microbiome, vol. 9, no. 1, 143. https://doi.org/10.1186/s40168-021-01087-w, https://doi.org/10.1186/s40168-021-01087-w

TY - JOUR

T1 - Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches

AU - Huws, Sharon A.

AU - Edwards, Joan E.

AU - Lin, Wanchang

AU - Rubino, Francesco

AU - Alston, Mark

AU - Swarbreck, David

AU - Caim, Shabhonam

AU - Stevens, Pauline Rees

AU - Pachebat, Justin

AU - Won, Mi-Young

AU - Oyama, Linda B.

AU - Creevey, Christopher J.

AU - Kingston-Smith, Alison H.

N1 - 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.

PY - 2021/12

Y1 - 2021/12

N2 - 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

AB - 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

KW - Archaea

KW - Bacteria

KW - Biofilm

KW - Colonisation

KW - Ecology

KW - Metatranscriptome

KW - Microbiome

KW - Niche

KW - Rumen

KW - Temporal

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U2 - 10.1186/s40168-021-01087-w

DO - 10.1186/s40168-021-01087-w

M3 - Article

C2 - 34154659

SN - 2049-2618

VL - 9

JO - Microbiome

JF - Microbiome

IS - 1

M1 - 143

ER -

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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

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