A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>

ABSTRACT Soil microbes produce an immense diversity of metabolites, including volatile organic compounds (VOCs), which can shape the structure and function of microbial communities. VOCs mediate a multitude of microbe-microbe interactions, including antagonism. Despite their importance, the diversit...

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Autores principales: Mallory Choudoir, Sam Rossabi, Matthew Gebert, Detlev Helmig, Noah Fierer
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Publicado: American Society for Microbiology 2019
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Acceso en línea:https://doaj.org/article/252b3857305942bdbd26bc0ecabea47d
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spelling oai:doaj.org-article:252b3857305942bdbd26bc0ecabea47d2021-12-02T19:47:34ZA Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>10.1128/mSystems.00295-182379-5077https://doaj.org/article/252b3857305942bdbd26bc0ecabea47d2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00295-18https://doaj.org/toc/2379-5077ABSTRACT Soil microbes produce an immense diversity of metabolites, including volatile organic compounds (VOCs), which can shape the structure and function of microbial communities. VOCs mediate a multitude of microbe-microbe interactions, including antagonism. Despite their importance, the diversity and functional relevance of most microbial volatiles remain uncharacterized. We assembled a taxonomically diverse collection of 48 Actinobacteria isolated from soil and airborne dust and surveyed the VOCs produced by these strains on two different medium types in vitro using gas chromatography-mass spectrometry (GC-MS). We detected 126 distinct VOCs and structurally identified approximately 20% of these compounds, which were predominately C1 to C5 hetero-VOCs, including (oxygenated) alcohols, ketones, esters, and nitrogen- and sulfur-containing compounds. Each strain produced a unique VOC profile. While the most common VOCs were likely by-products of primary metabolism, most of the VOCs were strain specific. We observed a strong taxonomic and phylogenetic signal for VOC profiles, suggesting their role in finer-scale patterns of ecological diversity. Finally, we investigated the functional potential of these VOCs by assessing their effects on growth rates of both pathogenic and nonpathogenic pseudomonad strains. We identified sets of VOCs that correlated with growth inhibition and stimulation, information that may facilitate the development of microbial VOC-based pathogen control strategies. IMPORTANCE Soil microbes produce a diverse array of natural products, including volatile organic compounds (VOCs). Volatile compounds are important molecules in soil habitats, where they mediate interactions between bacteria, fungi, insects, plants, and animals. We measured the VOCs produced by a broad diversity of soil- and dust-dwelling Actinobacteria in vitro. We detected a total of 126 unique volatile compounds, and each strain produced a unique combination of VOCs. While some of the compounds were produced by many strains, most were strain specific. Importantly, VOC profiles were more similar between closely related strains, indicating that evolutionary and ecological processes generate predictable patterns of VOC production. Finally, we observed that actinobacterial VOCs had both stimulatory and inhibitory effects on the growth of bacteria that represent a plant-beneficial symbiont and a plant-pathogenic strain, information that may lead to the development of novel strategies for plant disease prevention.Mallory ChoudoirSam RossabiMatthew GebertDetlev HelmigNoah FiererAmerican Society for MicrobiologyarticleActinobacteriaVOCactinomycetesmicrobial interactionsnatural productsvolatile organic compoundsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 2 (2019)
institution DOAJ
collection DOAJ
language EN
topic Actinobacteria
VOC
actinomycetes
microbial interactions
natural products
volatile organic compounds
Microbiology
QR1-502
spellingShingle Actinobacteria
VOC
actinomycetes
microbial interactions
natural products
volatile organic compounds
Microbiology
QR1-502
Mallory Choudoir
Sam Rossabi
Matthew Gebert
Detlev Helmig
Noah Fierer
A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
description ABSTRACT Soil microbes produce an immense diversity of metabolites, including volatile organic compounds (VOCs), which can shape the structure and function of microbial communities. VOCs mediate a multitude of microbe-microbe interactions, including antagonism. Despite their importance, the diversity and functional relevance of most microbial volatiles remain uncharacterized. We assembled a taxonomically diverse collection of 48 Actinobacteria isolated from soil and airborne dust and surveyed the VOCs produced by these strains on two different medium types in vitro using gas chromatography-mass spectrometry (GC-MS). We detected 126 distinct VOCs and structurally identified approximately 20% of these compounds, which were predominately C1 to C5 hetero-VOCs, including (oxygenated) alcohols, ketones, esters, and nitrogen- and sulfur-containing compounds. Each strain produced a unique VOC profile. While the most common VOCs were likely by-products of primary metabolism, most of the VOCs were strain specific. We observed a strong taxonomic and phylogenetic signal for VOC profiles, suggesting their role in finer-scale patterns of ecological diversity. Finally, we investigated the functional potential of these VOCs by assessing their effects on growth rates of both pathogenic and nonpathogenic pseudomonad strains. We identified sets of VOCs that correlated with growth inhibition and stimulation, information that may facilitate the development of microbial VOC-based pathogen control strategies. IMPORTANCE Soil microbes produce a diverse array of natural products, including volatile organic compounds (VOCs). Volatile compounds are important molecules in soil habitats, where they mediate interactions between bacteria, fungi, insects, plants, and animals. We measured the VOCs produced by a broad diversity of soil- and dust-dwelling Actinobacteria in vitro. We detected a total of 126 unique volatile compounds, and each strain produced a unique combination of VOCs. While some of the compounds were produced by many strains, most were strain specific. Importantly, VOC profiles were more similar between closely related strains, indicating that evolutionary and ecological processes generate predictable patterns of VOC production. Finally, we observed that actinobacterial VOCs had both stimulatory and inhibitory effects on the growth of bacteria that represent a plant-beneficial symbiont and a plant-pathogenic strain, information that may lead to the development of novel strategies for plant disease prevention.
format article
author Mallory Choudoir
Sam Rossabi
Matthew Gebert
Detlev Helmig
Noah Fierer
author_facet Mallory Choudoir
Sam Rossabi
Matthew Gebert
Detlev Helmig
Noah Fierer
author_sort Mallory Choudoir
title A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
title_short A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
title_full A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
title_fullStr A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
title_full_unstemmed A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by <italic toggle="yes">Actinobacteria</italic>
title_sort phylogenetic and functional perspective on volatile organic compound production by <italic toggle="yes">actinobacteria</italic>
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/252b3857305942bdbd26bc0ecabea47d
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