Cargando…

Can rumen bacteria communicate to each other?

BACKGROUND: The rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which then provide the host with energy and nutrients. Rumen microbes commonly attach to ingested plant materials and form biofilms for effective plant degradation. Quorum sensing (QS)...

Descripción completa

Detalles Bibliográficos
Autores principales: Won, Mi-Young, Oyama, Linda B., Courtney, Stephen J., Creevey, Christopher J., Huws, Sharon A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7035670/
https://www.ncbi.nlm.nih.gov/pubmed/32085816
http://dx.doi.org/10.1186/s40168-020-00796-y
_version_ 1783500101302353920
author Won, Mi-Young
Oyama, Linda B.
Courtney, Stephen J.
Creevey, Christopher J.
Huws, Sharon A.
author_facet Won, Mi-Young
Oyama, Linda B.
Courtney, Stephen J.
Creevey, Christopher J.
Huws, Sharon A.
author_sort Won, Mi-Young
collection PubMed
description BACKGROUND: The rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which then provide the host with energy and nutrients. Rumen microbes commonly attach to ingested plant materials and form biofilms for effective plant degradation. Quorum sensing (QS) is a well-recognised form of bacterial communication in most biofilm communities, with homoserine lactone (AHL)-based QS commonly being used by Gram-negative bacteria alone and AI-2 Lux-based QS communication being used to communicate across Gram-negative and Gram-positive bacteria. However, bacterial cell to cell communication in the rumen is poorly understood. In this study, rumen bacterial genomes from the Hungate collection and Genbank were prospected for QS-related genes. To check that the discovered QS genes are actually expressed in the rumen, we investigated expression levels in rumen metatranscriptome datasets. RESULTS: A total of 448 rumen bacterial genomes from the Hungate collection and Genbank, comprised of 311 Gram-positive, 136 Gram-negative and 1 Gram stain variable bacterium, were analysed. Abundance and distribution of AHL and AI-2 signalling genes showed that only one species (Citrobacter sp. NLAE-zl-C269) of a Gram-negative bacteria appeared to possess an AHL synthase gene, while the Lux-based genes (AI-2 QS) were identified in both Gram-positive and Gram-positive bacteria (191 genomes representing 38.2% of total genomes). Of these 192 genomes, 139 are from Gram-positive bactreetteria and 53 from Gram-negative bacteria. We also found that the genera Butyrivibrio, Prevotella, Ruminococcus and Pseudobutyrivibrio, which are well known as the most abundant bacterial genera in the rumen, possessed the most lux-based AI-2 QS genes. Gene expression levels within the metatranscriptome dataset showed that Prevotella, in particular, expressed high levels of LuxS synthase suggesting that this genus plays an important role in QS within the rumen. CONCLUSION: This is the most comprehensive study of QS in the rumen microbiome to date. This study shows that AI-2-based QS is rife in the rumen. These results allow a greater understanding on plant-microbe interactions in the rumen.
format Online
Article
Text
id pubmed-7035670
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-70356702020-02-27 Can rumen bacteria communicate to each other? Won, Mi-Young Oyama, Linda B. Courtney, Stephen J. Creevey, Christopher J. Huws, Sharon A. Microbiome Research BACKGROUND: The rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which then provide the host with energy and nutrients. Rumen microbes commonly attach to ingested plant materials and form biofilms for effective plant degradation. Quorum sensing (QS) is a well-recognised form of bacterial communication in most biofilm communities, with homoserine lactone (AHL)-based QS commonly being used by Gram-negative bacteria alone and AI-2 Lux-based QS communication being used to communicate across Gram-negative and Gram-positive bacteria. However, bacterial cell to cell communication in the rumen is poorly understood. In this study, rumen bacterial genomes from the Hungate collection and Genbank were prospected for QS-related genes. To check that the discovered QS genes are actually expressed in the rumen, we investigated expression levels in rumen metatranscriptome datasets. RESULTS: A total of 448 rumen bacterial genomes from the Hungate collection and Genbank, comprised of 311 Gram-positive, 136 Gram-negative and 1 Gram stain variable bacterium, were analysed. Abundance and distribution of AHL and AI-2 signalling genes showed that only one species (Citrobacter sp. NLAE-zl-C269) of a Gram-negative bacteria appeared to possess an AHL synthase gene, while the Lux-based genes (AI-2 QS) were identified in both Gram-positive and Gram-positive bacteria (191 genomes representing 38.2% of total genomes). Of these 192 genomes, 139 are from Gram-positive bactreetteria and 53 from Gram-negative bacteria. We also found that the genera Butyrivibrio, Prevotella, Ruminococcus and Pseudobutyrivibrio, which are well known as the most abundant bacterial genera in the rumen, possessed the most lux-based AI-2 QS genes. Gene expression levels within the metatranscriptome dataset showed that Prevotella, in particular, expressed high levels of LuxS synthase suggesting that this genus plays an important role in QS within the rumen. CONCLUSION: This is the most comprehensive study of QS in the rumen microbiome to date. This study shows that AI-2-based QS is rife in the rumen. These results allow a greater understanding on plant-microbe interactions in the rumen. BioMed Central 2020-02-21 /pmc/articles/PMC7035670/ /pubmed/32085816 http://dx.doi.org/10.1186/s40168-020-00796-y Text en © The Author(s) 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Won, Mi-Young
Oyama, Linda B.
Courtney, Stephen J.
Creevey, Christopher J.
Huws, Sharon A.
Can rumen bacteria communicate to each other?
title Can rumen bacteria communicate to each other?
title_full Can rumen bacteria communicate to each other?
title_fullStr Can rumen bacteria communicate to each other?
title_full_unstemmed Can rumen bacteria communicate to each other?
title_short Can rumen bacteria communicate to each other?
title_sort can rumen bacteria communicate to each other?
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7035670/
https://www.ncbi.nlm.nih.gov/pubmed/32085816
http://dx.doi.org/10.1186/s40168-020-00796-y
work_keys_str_mv AT wonmiyoung canrumenbacteriacommunicatetoeachother
AT oyamalindab canrumenbacteriacommunicatetoeachother
AT courtneystephenj canrumenbacteriacommunicatetoeachother
AT creeveychristopherj canrumenbacteriacommunicatetoeachother
AT huwssharona canrumenbacteriacommunicatetoeachother