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Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome

Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialized metabolites, including half of all known antibiotics. They are also rhizobacteria and plant endophytes that can promote plant growth and protect against disease. Several studies have shown that streptomyce...

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Autores principales: Worsley, Sarah F., Macey, Michael C., Prudence, Samuel M. M., Wilkinson, Barrie, Murrell, J. Colin, Hutchings, Matthew I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8241931/
https://www.ncbi.nlm.nih.gov/pubmed/34222338
http://dx.doi.org/10.3389/fmolb.2021.686110
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author Worsley, Sarah F.
Macey, Michael C.
Prudence, Samuel M. M.
Wilkinson, Barrie
Murrell, J. Colin
Hutchings, Matthew I.
author_facet Worsley, Sarah F.
Macey, Michael C.
Prudence, Samuel M. M.
Wilkinson, Barrie
Murrell, J. Colin
Hutchings, Matthew I.
author_sort Worsley, Sarah F.
collection PubMed
description Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialized metabolites, including half of all known antibiotics. They are also rhizobacteria and plant endophytes that can promote plant growth and protect against disease. Several studies have shown that streptomycetes are enriched in the rhizosphere and endosphere of the model plant Arabidopsis thaliana. Here, we set out to test the hypothesis that they are attracted to plant roots by root exudates, and specifically by the plant phytohormone salicylate, which they might use as a nutrient source. We confirmed a previously published report that salicylate over-producing cpr5 plants are colonized more readily by streptomycetes but found that salicylate-deficient sid2-2 and pad4 plants had the same levels of root colonization by Streptomyces bacteria as the wild-type plants. We then tested eight genome sequenced Streptomyces endophyte strains in vitro and found that none were attracted to or could grow on salicylate as a sole carbon source. We next used (13)CO(2) DNA stable isotope probing to test whether Streptomyces species can feed off a wider range of plant metabolites but found that Streptomyces bacteria were outcompeted by faster growing proteobacteria and did not incorporate photosynthetically fixed carbon into their DNA. We conclude that, given their saprotrophic nature and under conditions of high competition, streptomycetes most likely feed on more complex organic material shed by growing plant roots. Understanding the factors that impact the competitiveness of strains in the plant root microbiome could have consequences for the effective application of biocontrol strains.
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spelling pubmed-82419312021-07-01 Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome Worsley, Sarah F. Macey, Michael C. Prudence, Samuel M. M. Wilkinson, Barrie Murrell, J. Colin Hutchings, Matthew I. Front Mol Biosci Molecular Biosciences Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialized metabolites, including half of all known antibiotics. They are also rhizobacteria and plant endophytes that can promote plant growth and protect against disease. Several studies have shown that streptomycetes are enriched in the rhizosphere and endosphere of the model plant Arabidopsis thaliana. Here, we set out to test the hypothesis that they are attracted to plant roots by root exudates, and specifically by the plant phytohormone salicylate, which they might use as a nutrient source. We confirmed a previously published report that salicylate over-producing cpr5 plants are colonized more readily by streptomycetes but found that salicylate-deficient sid2-2 and pad4 plants had the same levels of root colonization by Streptomyces bacteria as the wild-type plants. We then tested eight genome sequenced Streptomyces endophyte strains in vitro and found that none were attracted to or could grow on salicylate as a sole carbon source. We next used (13)CO(2) DNA stable isotope probing to test whether Streptomyces species can feed off a wider range of plant metabolites but found that Streptomyces bacteria were outcompeted by faster growing proteobacteria and did not incorporate photosynthetically fixed carbon into their DNA. We conclude that, given their saprotrophic nature and under conditions of high competition, streptomycetes most likely feed on more complex organic material shed by growing plant roots. Understanding the factors that impact the competitiveness of strains in the plant root microbiome could have consequences for the effective application of biocontrol strains. Frontiers Media S.A. 2021-06-16 /pmc/articles/PMC8241931/ /pubmed/34222338 http://dx.doi.org/10.3389/fmolb.2021.686110 Text en Copyright © 2021 Worsley, Macey, Prudence, Wilkinson, Murrell and Hutchings. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Biosciences
Worsley, Sarah F.
Macey, Michael C.
Prudence, Samuel M. M.
Wilkinson, Barrie
Murrell, J. Colin
Hutchings, Matthew I.
Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title_full Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title_fullStr Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title_full_unstemmed Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title_short Investigating the Role of Root Exudates in Recruiting Streptomyces Bacteria to the Arabidopsis thaliana Microbiome
title_sort investigating the role of root exudates in recruiting streptomyces bacteria to the arabidopsis thaliana microbiome
topic Molecular Biosciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8241931/
https://www.ncbi.nlm.nih.gov/pubmed/34222338
http://dx.doi.org/10.3389/fmolb.2021.686110
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