Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome

ABSTRACT Soils host diverse microbial communities that include filamentous actinobacteria (actinomycetes). These bacteria have been a rich source of useful metabolites, including antimicrobials, antifungals, anticancer agents, siderophores, and immunosuppressants. While humans have long exploited th...

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Autores principales:	Matthew F. Traxler, Jeramie D. Watrous, Theodore Alexandrov, Pieter C. Dorrestein, Roberto Kolter
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9fcd565fb46f4855bbdf6de034caf5dc
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spelling	oai:doaj.org-article:9fcd565fb46f4855bbdf6de034caf5dc2021-11-15T15:43:08ZInterspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome10.1128/mBio.00459-132150-7511https://doaj.org/article/9fcd565fb46f4855bbdf6de034caf5dc2013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00459-13https://doaj.org/toc/2150-7511ABSTRACT Soils host diverse microbial communities that include filamentous actinobacteria (actinomycetes). These bacteria have been a rich source of useful metabolites, including antimicrobials, antifungals, anticancer agents, siderophores, and immunosuppressants. While humans have long exploited these compounds for therapeutic purposes, the role these natural products may play in mediating interactions between actinomycetes has been difficult to ascertain. As an initial step toward understanding these chemical interactions at a systems level, we employed the emerging techniques of nanospray desorption electrospray ionization (NanoDESI) and matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry to gain a global chemical view of the model bacterium Streptomyces coelicolor interacting with five other actinomycetes. In each interaction, the majority of secreted compounds associated with S. coelicolor colonies were unique, suggesting an idiosyncratic response from S. coelicolor. Spectral networking revealed a family of unknown compounds produced by S. coelicolor during several interactions. These compounds constitute an extended suite of at least 12 different desferrioxamines with acyl side chains of various lengths; their production was triggered by siderophores made by neighboring strains. Taken together, these results illustrate that chemical interactions between actinomycete bacteria exhibit high complexity and specificity and can drive differential secondary metabolite production. IMPORTANCE Actinomycetes, filamentous actinobacteria from the soil, are the deepest natural source of useful medicinal compounds, including antibiotics, antifungals, and anticancer agents. There is great interest in developing new strategies that increase the diversity of metabolites secreted by actinomycetes in the laboratory. Here we used several metabolomic approaches to examine the chemicals made by these bacteria when grown in pairwise coculture. We found that these interspecies interactions stimulated production of numerous chemical compounds that were not made when they grew alone. Among these compounds were at least 12 different versions of a molecule called desferrioxamine, a siderophore used by the bacteria to gather iron. Many other compounds of unknown identity were also observed, and the pattern of compound production varied greatly among the interaction sets. These findings suggest that chemical interactions between actinomycetes are surprisingly complex and that coculture may be a promising strategy for finding new molecules from actinomycetes.Matthew F. TraxlerJeramie D. WatrousTheodore AlexandrovPieter C. DorresteinRoberto KolterAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Matthew F. Traxler Jeramie D. Watrous Theodore Alexandrov Pieter C. Dorrestein Roberto Kolter Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
description	ABSTRACT Soils host diverse microbial communities that include filamentous actinobacteria (actinomycetes). These bacteria have been a rich source of useful metabolites, including antimicrobials, antifungals, anticancer agents, siderophores, and immunosuppressants. While humans have long exploited these compounds for therapeutic purposes, the role these natural products may play in mediating interactions between actinomycetes has been difficult to ascertain. As an initial step toward understanding these chemical interactions at a systems level, we employed the emerging techniques of nanospray desorption electrospray ionization (NanoDESI) and matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry to gain a global chemical view of the model bacterium Streptomyces coelicolor interacting with five other actinomycetes. In each interaction, the majority of secreted compounds associated with S. coelicolor colonies were unique, suggesting an idiosyncratic response from S. coelicolor. Spectral networking revealed a family of unknown compounds produced by S. coelicolor during several interactions. These compounds constitute an extended suite of at least 12 different desferrioxamines with acyl side chains of various lengths; their production was triggered by siderophores made by neighboring strains. Taken together, these results illustrate that chemical interactions between actinomycete bacteria exhibit high complexity and specificity and can drive differential secondary metabolite production. IMPORTANCE Actinomycetes, filamentous actinobacteria from the soil, are the deepest natural source of useful medicinal compounds, including antibiotics, antifungals, and anticancer agents. There is great interest in developing new strategies that increase the diversity of metabolites secreted by actinomycetes in the laboratory. Here we used several metabolomic approaches to examine the chemicals made by these bacteria when grown in pairwise coculture. We found that these interspecies interactions stimulated production of numerous chemical compounds that were not made when they grew alone. Among these compounds were at least 12 different versions of a molecule called desferrioxamine, a siderophore used by the bacteria to gather iron. Many other compounds of unknown identity were also observed, and the pattern of compound production varied greatly among the interaction sets. These findings suggest that chemical interactions between actinomycetes are surprisingly complex and that coculture may be a promising strategy for finding new molecules from actinomycetes.
format	article
author	Matthew F. Traxler Jeramie D. Watrous Theodore Alexandrov Pieter C. Dorrestein Roberto Kolter
author_facet	Matthew F. Traxler Jeramie D. Watrous Theodore Alexandrov Pieter C. Dorrestein Roberto Kolter
author_sort	Matthew F. Traxler
title	Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
title_short	Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
title_full	Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
title_fullStr	Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
title_full_unstemmed	Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome
title_sort	interspecies interactions stimulate diversification of the <named-content content-type="genus-species">streptomyces coelicolor</named-content> secreted metabolome
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/9fcd565fb46f4855bbdf6de034caf5dc
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Interspecies Interactions Stimulate Diversification of the <named-content content-type="genus-species">Streptomyces coelicolor</named-content> Secreted Metabolome

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