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Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces

Though traditionally perceived as weapons, antibiotics are also hypothesized to act as microbial signals in natural habitats. However, while subinhibitory concentrations of antibiotics (SICA) are known to shift bacterial gene expression, specific hypotheses as to how SICA influence the ecology of na...

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Autores principales: Vaz Jauri, Patricia, Bakker, Matthew G., Salomon, Christine E., Kinkel, Linda L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3855208/
https://www.ncbi.nlm.nih.gov/pubmed/24339897
http://dx.doi.org/10.1371/journal.pone.0081064
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author Vaz Jauri, Patricia
Bakker, Matthew G.
Salomon, Christine E.
Kinkel, Linda L.
author_facet Vaz Jauri, Patricia
Bakker, Matthew G.
Salomon, Christine E.
Kinkel, Linda L.
author_sort Vaz Jauri, Patricia
collection PubMed
description Though traditionally perceived as weapons, antibiotics are also hypothesized to act as microbial signals in natural habitats. However, while subinhibitory concentrations of antibiotics (SICA) are known to shift bacterial gene expression, specific hypotheses as to how SICA influence the ecology of natural populations are scarce. We explored whether antibiotic ‘signals’, or SICA, have the potential to alter nutrient utilization, niche overlap, and competitive species interactions among Streptomyces populations in soil. For nine diverse Streptomyces isolates, we evaluated nutrient utilization patterns on 95 different nutrient sources in the presence and absence of subinhibitory concentrations of five antibiotics. There were significant changes in nutrient use among Streptomyces isolates, including both increases and decreases in the capacity to use individual nutrients in the presence vs. in the absence of SICA. Isolates varied in their responses to SICA and antibiotics varied in their effects on isolates. Furthermore, for some isolate-isolate-antibiotic combinations, competition-free growth (growth for an isolate on all nutrients that were not utilized by a competing isolate), was increased in the presence of SICA, reducing the potential fitness cost of nutrient competition among those competitors. This suggests that antibiotics may provide a mechanism for bacteria to actively minimize niche overlap among competitors in soil. Thus, in contrast to antagonistic coevolutionary dynamics, antibiotics as signals may mediate coevolutionary displacement among coexisting Streptomyces, thereby hindering the emergence of antibiotic resistant phenotypes. These results contribute to our broad understanding of the ecology and evolutionary biology of antibiotics and microbial signals in nature.
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spelling pubmed-38552082013-12-11 Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces Vaz Jauri, Patricia Bakker, Matthew G. Salomon, Christine E. Kinkel, Linda L. PLoS One Research Article Though traditionally perceived as weapons, antibiotics are also hypothesized to act as microbial signals in natural habitats. However, while subinhibitory concentrations of antibiotics (SICA) are known to shift bacterial gene expression, specific hypotheses as to how SICA influence the ecology of natural populations are scarce. We explored whether antibiotic ‘signals’, or SICA, have the potential to alter nutrient utilization, niche overlap, and competitive species interactions among Streptomyces populations in soil. For nine diverse Streptomyces isolates, we evaluated nutrient utilization patterns on 95 different nutrient sources in the presence and absence of subinhibitory concentrations of five antibiotics. There were significant changes in nutrient use among Streptomyces isolates, including both increases and decreases in the capacity to use individual nutrients in the presence vs. in the absence of SICA. Isolates varied in their responses to SICA and antibiotics varied in their effects on isolates. Furthermore, for some isolate-isolate-antibiotic combinations, competition-free growth (growth for an isolate on all nutrients that were not utilized by a competing isolate), was increased in the presence of SICA, reducing the potential fitness cost of nutrient competition among those competitors. This suggests that antibiotics may provide a mechanism for bacteria to actively minimize niche overlap among competitors in soil. Thus, in contrast to antagonistic coevolutionary dynamics, antibiotics as signals may mediate coevolutionary displacement among coexisting Streptomyces, thereby hindering the emergence of antibiotic resistant phenotypes. These results contribute to our broad understanding of the ecology and evolutionary biology of antibiotics and microbial signals in nature. Public Library of Science 2013-12-05 /pmc/articles/PMC3855208/ /pubmed/24339897 http://dx.doi.org/10.1371/journal.pone.0081064 Text en © 2013 Vaz Jauri et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Vaz Jauri, Patricia
Bakker, Matthew G.
Salomon, Christine E.
Kinkel, Linda L.
Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title_full Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title_fullStr Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title_full_unstemmed Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title_short Subinhibitory Antibiotic Concentrations Mediate Nutrient Use and Competition among Soil Streptomyces
title_sort subinhibitory antibiotic concentrations mediate nutrient use and competition among soil streptomyces
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3855208/
https://www.ncbi.nlm.nih.gov/pubmed/24339897
http://dx.doi.org/10.1371/journal.pone.0081064
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