Cargando…

Spatial structure increases the benefits of antibiotic production in Streptomyces

Bacteria in the soil compete for limited resources. One of the ways they might do this is by producing antibiotics, but the metabolic costs of antibiotics and their low concentrations have caused uncertainty about the ecological role of these products for the bacteria that produce them. Here, we exa...

Descripción completa

Detalles Bibliográficos
Autores principales: Westhoff, Sanne, Otto, Simon B., Swinkels, Aram, Bode, Bo, van Wezel, Gilles P., Rozen, Daniel E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6973283/
https://www.ncbi.nlm.nih.gov/pubmed/31393002
http://dx.doi.org/10.1111/evo.13817
_version_ 1783490012017328128
author Westhoff, Sanne
Otto, Simon B.
Swinkels, Aram
Bode, Bo
van Wezel, Gilles P.
Rozen, Daniel E.
author_facet Westhoff, Sanne
Otto, Simon B.
Swinkels, Aram
Bode, Bo
van Wezel, Gilles P.
Rozen, Daniel E.
author_sort Westhoff, Sanne
collection PubMed
description Bacteria in the soil compete for limited resources. One of the ways they might do this is by producing antibiotics, but the metabolic costs of antibiotics and their low concentrations have caused uncertainty about the ecological role of these products for the bacteria that produce them. Here, we examine the benefits of streptomycin production by the filamentous bacterium Streptomyces griseus. We first provide evidence that streptomycin production enables S. griseus to kill and invade the susceptible species, S. coelicolor, but not a streptomycin‐resistant mutant of this species. Next, we show that the benefits of streptomycin production are density dependent, because production scales positively with cell number, and frequency dependent, with a threshold of invasion of S. griseus at around 1%. Finally, using serial transfer experiments where spatial structure is either maintained or destroyed, we show that spatial structure reduces the threshold frequency of invasion by more than 100‐fold, indicating that antibiotic production can permit invasion from extreme rarity. Our results show that streptomycin is both an offensive and defensive weapon that facilitates invasion into occupied habitats and also protects against invasion by competitors. They also indicate that the benefits of antibiotic production rely on ecological interactions occurring at small local scales.
format Online
Article
Text
id pubmed-6973283
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-69732832020-01-28 Spatial structure increases the benefits of antibiotic production in Streptomyces Westhoff, Sanne Otto, Simon B. Swinkels, Aram Bode, Bo van Wezel, Gilles P. Rozen, Daniel E. Evolution Brief Communications Bacteria in the soil compete for limited resources. One of the ways they might do this is by producing antibiotics, but the metabolic costs of antibiotics and their low concentrations have caused uncertainty about the ecological role of these products for the bacteria that produce them. Here, we examine the benefits of streptomycin production by the filamentous bacterium Streptomyces griseus. We first provide evidence that streptomycin production enables S. griseus to kill and invade the susceptible species, S. coelicolor, but not a streptomycin‐resistant mutant of this species. Next, we show that the benefits of streptomycin production are density dependent, because production scales positively with cell number, and frequency dependent, with a threshold of invasion of S. griseus at around 1%. Finally, using serial transfer experiments where spatial structure is either maintained or destroyed, we show that spatial structure reduces the threshold frequency of invasion by more than 100‐fold, indicating that antibiotic production can permit invasion from extreme rarity. Our results show that streptomycin is both an offensive and defensive weapon that facilitates invasion into occupied habitats and also protects against invasion by competitors. They also indicate that the benefits of antibiotic production rely on ecological interactions occurring at small local scales. John Wiley and Sons Inc. 2019-08-26 2020-01 /pmc/articles/PMC6973283/ /pubmed/31393002 http://dx.doi.org/10.1111/evo.13817 Text en © 2019 The Authors. Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Brief Communications
Westhoff, Sanne
Otto, Simon B.
Swinkels, Aram
Bode, Bo
van Wezel, Gilles P.
Rozen, Daniel E.
Spatial structure increases the benefits of antibiotic production in Streptomyces
title Spatial structure increases the benefits of antibiotic production in Streptomyces
title_full Spatial structure increases the benefits of antibiotic production in Streptomyces
title_fullStr Spatial structure increases the benefits of antibiotic production in Streptomyces
title_full_unstemmed Spatial structure increases the benefits of antibiotic production in Streptomyces
title_short Spatial structure increases the benefits of antibiotic production in Streptomyces
title_sort spatial structure increases the benefits of antibiotic production in streptomyces
topic Brief Communications
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6973283/
https://www.ncbi.nlm.nih.gov/pubmed/31393002
http://dx.doi.org/10.1111/evo.13817
work_keys_str_mv AT westhoffsanne spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces
AT ottosimonb spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces
AT swinkelsaram spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces
AT bodebo spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces
AT vanwezelgillesp spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces
AT rozendaniele spatialstructureincreasesthebenefitsofantibioticproductioninstreptomyces