A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by Actinobacteria

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 48Actinobacteriaisolated from soil and airborne dust and surveyed the VOCs produced by these strains on two different medium typesin vitrousing gas chromatography-mass spectrometry (GC-MS). We detected 126 distinct VOCs and structurally identified approximately 20% of these compounds, which were predominately C1to C5hetero-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.IMPORTANCESoil 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-dwellingActinobacteria 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.

Identification of Rhizospheric Actinomycete Streptomyces lavendulae SPS-33 and the Inhibitory Effect of its Volatile Organic Compounds against Ceratocystis fimbriata in Postharvest Sweet Potato (Ipomoea batatas (L.) Lam.)

“…These three volatiles have good antimicrobial activity and can be produced by a variety of microorganisms, such as S. fimicarius BWL-H1, different Actinobacteria isolates, and Pseudomonas chlororaphis subsp. aureofaciens SPS-41 [20,49,50]. It was found that alcohols showed a noticeably higher antimicrobial activity than esters and ketones in this study, which was consistent with other reports [9,20].…”

“…cultured on Emmerson's yeast starch agar, the most common compounds included isoprene, acetone, 3-methyl-1-butanol, 2-methyl-1-butanol, cyclopentanone, dimethyl disulfide, dimethyl trisulfide, phenylethyl alcohol, and geosmin [48]. It was indicated that some frequently produced VOCs may be the by-products of primary metabolism [49] like an earthy-smelling substance geosmin [34]. However, most of the VOCs are strain-specific, which means each strain produces a unique profile of VOCs [49].…”

“…It was indicated that some frequently produced VOCs may be the by-products of primary metabolism [49] like an earthy-smelling substance geosmin [34]. However, most of the VOCs are strain-specific, which means each strain produces a unique profile of VOCs [49]. The VOCs produced by streptomycetes generally include alcohols, esters, ketones, sulfur compounds, and terpenoid compounds [48].…”

Dimethyl disulfide exerts antifungal activity against Sclerotinia minor by damaging its membrane and induces systemic resistance in host plants

“…However, an understanding of the mechanisms underlying the effects of these compounds and studies on their application in situ has been limited although there are a few reports for action mode such as DNA damage by N-methyl-N-nitrosoisobutyramide generated from fungi 23,24 . In nature, MVCs are produced as mixtures of several compounds in which the composition and concentration of each compound is not well defined and differs in the producing microorganisms, depending on the nutrient availability and metabolic activity 9,22,25,26 . Although MVCs can act as multitrophic signals in ecologically complex systems and can elicit pleiotropic responses 25,26 , the practical application of MVCs as alternatives to chemical pesticides requires more information, such as accurate identification and assessment of the bioactive compounds.…”

In Vivo Studies of Inoculated Plants and In Vitro Studies Utilizing Methanolic Extracts of Endophytic Streptomyces sp. Strain DBT34 Obtained from Mirabilis jalapa L. Exhibit ROS-Scavenging and Other Bioactive Properties

“…GC-MS analysis is an excellent method to detect and identify VOCs and has been used by several researchers to identify VOCs [ 35 ]. VOCs, including alcohol, ketones, esters, acetic acid groups, amides, and their derivatives, have been detected in genera of Actinobacteria [ 36 ]. In the present study, 11 volatile compounds were detected in the methanolic extract of Streptomyces sp.…”