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A competitive trade-off limits the selective advantage of increased antibiotic production

In structured environments, antibiotic producing microorganisms can gain a selective advantage by inhibiting nearby competing species(1). However, despite their genetic potential(2,3), natural isolates often make only small amounts of antibiotics, and laboratory evolution can lead to loss rather tha...

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Detalles Bibliográficos
Autores principales: Gerardin, Ylaine, Springer, Michael, Kishony, Roy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5046839/
https://www.ncbi.nlm.nih.gov/pubmed/27668360
http://dx.doi.org/10.1038/nmicrobiol.2016.175
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author Gerardin, Ylaine
Springer, Michael
Kishony, Roy
author_facet Gerardin, Ylaine
Springer, Michael
Kishony, Roy
author_sort Gerardin, Ylaine
collection PubMed
description In structured environments, antibiotic producing microorganisms can gain a selective advantage by inhibiting nearby competing species(1). However, despite their genetic potential(2,3), natural isolates often make only small amounts of antibiotics, and laboratory evolution can lead to loss rather than enhancement of antibiotic production(4). Here we show that, due to competition with antibiotic resistant cheater cells, increased levels of antibiotic production can actually decrease the selective advantage to producers. Competing fluorescently-labeled Escherichia coli colicin producers with non-producing resistant and sensitive strains on solid media, we found that while producer colonies can greatly benefit from the inhibition of nearby sensitive colonies, this benefit is shared with resistant colonies growing in their vicinity. A simple model, which accounts for such local competitive and inhibitory interactions, suggests that the advantage of producers varies non-monotonically with the amount of production. Indeed, experimentally varying the amount of production shows a peak in selection for producers, reflecting a trade-off between benefit gained by inhibiting sensitive competitors and loss due to an increased contribution to resistant cheater colonies. These results help explain the low level of antibiotic production observed for natural species, and can help direct laboratory evolution experiments selecting for increased or novel production of antibiotics.
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spelling pubmed-50468392017-03-26 A competitive trade-off limits the selective advantage of increased antibiotic production Gerardin, Ylaine Springer, Michael Kishony, Roy Nat Microbiol Article In structured environments, antibiotic producing microorganisms can gain a selective advantage by inhibiting nearby competing species(1). However, despite their genetic potential(2,3), natural isolates often make only small amounts of antibiotics, and laboratory evolution can lead to loss rather than enhancement of antibiotic production(4). Here we show that, due to competition with antibiotic resistant cheater cells, increased levels of antibiotic production can actually decrease the selective advantage to producers. Competing fluorescently-labeled Escherichia coli colicin producers with non-producing resistant and sensitive strains on solid media, we found that while producer colonies can greatly benefit from the inhibition of nearby sensitive colonies, this benefit is shared with resistant colonies growing in their vicinity. A simple model, which accounts for such local competitive and inhibitory interactions, suggests that the advantage of producers varies non-monotonically with the amount of production. Indeed, experimentally varying the amount of production shows a peak in selection for producers, reflecting a trade-off between benefit gained by inhibiting sensitive competitors and loss due to an increased contribution to resistant cheater colonies. These results help explain the low level of antibiotic production observed for natural species, and can help direct laboratory evolution experiments selecting for increased or novel production of antibiotics. 2016-09-26 /pmc/articles/PMC5046839/ /pubmed/27668360 http://dx.doi.org/10.1038/nmicrobiol.2016.175 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Gerardin, Ylaine
Springer, Michael
Kishony, Roy
A competitive trade-off limits the selective advantage of increased antibiotic production
title A competitive trade-off limits the selective advantage of increased antibiotic production
title_full A competitive trade-off limits the selective advantage of increased antibiotic production
title_fullStr A competitive trade-off limits the selective advantage of increased antibiotic production
title_full_unstemmed A competitive trade-off limits the selective advantage of increased antibiotic production
title_short A competitive trade-off limits the selective advantage of increased antibiotic production
title_sort competitive trade-off limits the selective advantage of increased antibiotic production
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5046839/
https://www.ncbi.nlm.nih.gov/pubmed/27668360
http://dx.doi.org/10.1038/nmicrobiol.2016.175
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