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Community composition drives siderophore dynamics in multispecies bacterial communities

BACKGROUND: Intraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope recepto...

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Autores principales: O’Brien, Siobhán, Culbert, Christopher T., Barraclough, Timothy G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10472669/
https://www.ncbi.nlm.nih.gov/pubmed/37658316
http://dx.doi.org/10.1186/s12862-023-02152-8
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author O’Brien, Siobhán
Culbert, Christopher T.
Barraclough, Timothy G.
author_facet O’Brien, Siobhán
Culbert, Christopher T.
Barraclough, Timothy G.
author_sort O’Brien, Siobhán
collection PubMed
description BACKGROUND: Intraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope receptor and transport systems. Intraspecific social exploitation of siderophore producers is common, since non-producers avoid the costs of production but retain the cell envelope machinery for siderophore uptake. However, little is known about how interactions between species (i.e., interspecific interactions) can shape intraspecific public goods exploitation. Here, we predicted that strong competition for iron between species in diverse communities will increase costs of siderophore cooperation, and hence drive intraspecific exploitation. We examined how increasing microbial community species diversity shapes intraspecific social dynamics by monitoring the growth of siderophore producers and non-producers of the plant-growth promoting bacterium Pseudomonas fluorescens, embedded within tree-hole microbial communities ranging from 2 to 15 species. RESULTS: We find, contrary to our prediction, that siderophore production is favoured at higher levels of community species richness, driven by increased likelihood of encountering key species that reduce the growth of siderophore non-producing (but not producing) strains of P. fluorescens. CONCLUSIONS: Our results suggest that maintaining a diverse soil microbiota could partly contribute to the maintenance of siderophore production in natural communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02152-8.
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spelling pubmed-104726692023-09-02 Community composition drives siderophore dynamics in multispecies bacterial communities O’Brien, Siobhán Culbert, Christopher T. Barraclough, Timothy G. BMC Ecol Evol Research BACKGROUND: Intraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope receptor and transport systems. Intraspecific social exploitation of siderophore producers is common, since non-producers avoid the costs of production but retain the cell envelope machinery for siderophore uptake. However, little is known about how interactions between species (i.e., interspecific interactions) can shape intraspecific public goods exploitation. Here, we predicted that strong competition for iron between species in diverse communities will increase costs of siderophore cooperation, and hence drive intraspecific exploitation. We examined how increasing microbial community species diversity shapes intraspecific social dynamics by monitoring the growth of siderophore producers and non-producers of the plant-growth promoting bacterium Pseudomonas fluorescens, embedded within tree-hole microbial communities ranging from 2 to 15 species. RESULTS: We find, contrary to our prediction, that siderophore production is favoured at higher levels of community species richness, driven by increased likelihood of encountering key species that reduce the growth of siderophore non-producing (but not producing) strains of P. fluorescens. CONCLUSIONS: Our results suggest that maintaining a diverse soil microbiota could partly contribute to the maintenance of siderophore production in natural communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02152-8. BioMed Central 2023-09-01 /pmc/articles/PMC10472669/ /pubmed/37658316 http://dx.doi.org/10.1186/s12862-023-02152-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
O’Brien, Siobhán
Culbert, Christopher T.
Barraclough, Timothy G.
Community composition drives siderophore dynamics in multispecies bacterial communities
title Community composition drives siderophore dynamics in multispecies bacterial communities
title_full Community composition drives siderophore dynamics in multispecies bacterial communities
title_fullStr Community composition drives siderophore dynamics in multispecies bacterial communities
title_full_unstemmed Community composition drives siderophore dynamics in multispecies bacterial communities
title_short Community composition drives siderophore dynamics in multispecies bacterial communities
title_sort community composition drives siderophore dynamics in multispecies bacterial communities
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10472669/
https://www.ncbi.nlm.nih.gov/pubmed/37658316
http://dx.doi.org/10.1186/s12862-023-02152-8
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