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Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community

BACKGROUND: Antagonistic interactions mediated by antibiotics are strong drivers of bacterial community dynamics which shape biodiversity. Colicin production by Escherichia coli is such an interaction that governs intraspecific competition and is involved in promoting biodiversity. It is unknown how...

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Autores principales: Hol, Felix JH, Voges, Mathias J, Dekker, Cees, Keymer, Juan E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161892/
https://www.ncbi.nlm.nih.gov/pubmed/25159553
http://dx.doi.org/10.1186/s12915-014-0068-2
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author Hol, Felix JH
Voges, Mathias J
Dekker, Cees
Keymer, Juan E
author_facet Hol, Felix JH
Voges, Mathias J
Dekker, Cees
Keymer, Juan E
author_sort Hol, Felix JH
collection PubMed
description BACKGROUND: Antagonistic interactions mediated by antibiotics are strong drivers of bacterial community dynamics which shape biodiversity. Colicin production by Escherichia coli is such an interaction that governs intraspecific competition and is involved in promoting biodiversity. It is unknown how environmental cues affect regulation of the colicin operon and thus influence antibiotic-mediated community dynamics. RESULTS: Here, we investigate the community dynamics of colicin-producing, -sensitive, and -resistant/non-producer E. coli strains that colonize a microfabricated spatially-structured habitat. Nutrients are found to strongly influence community dynamics: when growing on amino acids and peptides, colicin-mediated competition is intense and the three strains do not coexist unless spatially separated at large scales (millimeters). Surprisingly, when growing on sugars, colicin-mediated competition is minimal and the three strains coexist at the micrometer scale. Carbon storage regulator A (CsrA) is found to play a key role in translating the type of nutrients into the observed community dynamics by controlling colicin release. We demonstrate that by mitigating lysis, CsrA shapes the community dynamics and determines whether the three strains coexist. Indeed, a mutant producer that is unable to suppress colicin release, causes the collapse of biodiversity in media that would otherwise support co-localized growth of the three strains. CONCLUSIONS: Our results show how the environmental regulation of an antagonistic trait shapes community dynamics. We demonstrate that nutrient-responsive regulation of colicin release by CsrA, determines whether colicin producer, resistant non-producer, and sensitive strains coexist at small spatial scales, or whether the sensitive strain is eradicated. This study highlights how molecular-level regulatory mechanisms that govern interference competition give rise to community-level biodiversity patterns. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0068-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-41618922014-09-25 Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community Hol, Felix JH Voges, Mathias J Dekker, Cees Keymer, Juan E BMC Biol Research Article BACKGROUND: Antagonistic interactions mediated by antibiotics are strong drivers of bacterial community dynamics which shape biodiversity. Colicin production by Escherichia coli is such an interaction that governs intraspecific competition and is involved in promoting biodiversity. It is unknown how environmental cues affect regulation of the colicin operon and thus influence antibiotic-mediated community dynamics. RESULTS: Here, we investigate the community dynamics of colicin-producing, -sensitive, and -resistant/non-producer E. coli strains that colonize a microfabricated spatially-structured habitat. Nutrients are found to strongly influence community dynamics: when growing on amino acids and peptides, colicin-mediated competition is intense and the three strains do not coexist unless spatially separated at large scales (millimeters). Surprisingly, when growing on sugars, colicin-mediated competition is minimal and the three strains coexist at the micrometer scale. Carbon storage regulator A (CsrA) is found to play a key role in translating the type of nutrients into the observed community dynamics by controlling colicin release. We demonstrate that by mitigating lysis, CsrA shapes the community dynamics and determines whether the three strains coexist. Indeed, a mutant producer that is unable to suppress colicin release, causes the collapse of biodiversity in media that would otherwise support co-localized growth of the three strains. CONCLUSIONS: Our results show how the environmental regulation of an antagonistic trait shapes community dynamics. We demonstrate that nutrient-responsive regulation of colicin release by CsrA, determines whether colicin producer, resistant non-producer, and sensitive strains coexist at small spatial scales, or whether the sensitive strain is eradicated. This study highlights how molecular-level regulatory mechanisms that govern interference competition give rise to community-level biodiversity patterns. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0068-2) contains supplementary material, which is available to authorized users. BioMed Central 2014-08-27 /pmc/articles/PMC4161892/ /pubmed/25159553 http://dx.doi.org/10.1186/s12915-014-0068-2 Text en © Hol et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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 Article
Hol, Felix JH
Voges, Mathias J
Dekker, Cees
Keymer, Juan E
Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title_full Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title_fullStr Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title_full_unstemmed Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title_short Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
title_sort nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161892/
https://www.ncbi.nlm.nih.gov/pubmed/25159553
http://dx.doi.org/10.1186/s12915-014-0068-2
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AT keymerjuane nutrientresponsiveregulationdeterminesbiodiversityinacolicinmediatedbacterialcommunity