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. 2023 Jul 16;11(7):1820.
doi: 10.3390/microorganisms11071820.

The Volatile Organic Compounds of Streptomyces spp.: An In-Depth Analysis of Their Antifungal Properties

Lorena Cuervo  1   2   3 , Samuel Álvarez-García  4 , José A Salas  1   2   3 , Carmen Méndez  1   2   3 , Carlos Olano  1   2   3 , Mónica G Malmierca  1   2   3
Affiliations

The Volatile Organic Compounds of Streptomyces spp.: An In-Depth Analysis of Their Antifungal Properties

Lorena Cuervo et al. Microorganisms. .

Abstract

The study of volatile organic compounds (VOCs) has expanded because of the growing need to search for new bioactive compounds that could be used as therapeutic alternatives. These small molecules serve as signals to establish interactions with other nearby organisms in the environment. In this work, we evaluated the antifungal effect of VOCs produced by different Streptomyces spp. This study was performed using VOC chamber devices that allow for the free exchange of VOCs without physical contact between microorganisms or the diffusible compounds they produce. Antifungal activity was tested against Escovopsis weberi, a fungal pathogen that affects ant nest stability, and the results showed that Streptomyces spp. CS014, CS057, CS131, CS147, CS159, CS207, and CS227 inhibit or reduce the fungal growth with their emitted VOCs. A GS-MS analysis of volatiles produced and captured by activated charcoal suggested that these Streptomyces strains synthesize several antifungal VOCs, many of them produced because of the presence of E. weberi, with the accumulation of various VOCs determining the growth inhibition effect.

Keywords: Escovopsis weberi; GS-MS; Streptomyces; antifungal; secondary metabolism; volatile organic compounds.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Volatile organic compound (VOC) chamber. (a) Schematic side view of a VOC chamber; (b) representation of each part of the VOC chamber device. The hole in the middle allows for the exchange of VOCs between cultures (modified from [16]); (c) photographs of an assembled VOC chamber (without charcoal).
Figure 2
Figure 2
Antifungal effect of Streptomyces’s volatile organic compounds (VOCs) on Escovopsis weberi. From left to right, E. weberi plate when cocultured in VOC chambers against Streptomyces spp. CS227, CS131, CS014, CS057 (first row), CS207, CS147, and CS159 (second row) grown on soy flour mannitol (SFM) medium. As a control for the assay, the last image corresponds to a VOC chamber without a Streptomyces sp. culture.
Figure 3
Figure 3
Average growth inhibition of Escovopsis weberi (n = 3) when cocultured with different Streptomyces sp. strains. Strains CS057, CS131, and CS227 cause inhibition above 90%. The standard deviation of the results is represented.
Figure 4
Figure 4
Upset Plot from the compounds detected via GS-MS from the assay confronting Streptomyces sp. CS057 and Escovopsis weberi. Ew: volatiles produced by E. weberi; SFMc: volatile produced during the coculture of E. weberi–Streptomyces sp. CS057 on soy flour mannitol (SFM) medium; SFM057: volatiles produced by CS57 on SFM; R5A57: volatiles produced by CS057 on R5A medium; R5Ac: volatiles produced during the coculture of E. weberi–Streptomyces sp. CS057 on R5A.
Figure 5
Figure 5
Upset Plot from the compounds detected via GS-MS from the assay confronting Streptomyces sp. CS131 and Escovopsis weberi. Ew: volatiles produced by E. weberi; SFMc: volatile produced during the coculture of E. weberi–Streptomyces sp. CS131 on soy flour mannitol (SFM) medium; SFM131: volatiles produced by CS131 on SFM; R5A131: volatiles produced by CS131 on R5A medium; R5Ac: volatiles produced during the coculture of E.weberi–Streptomyces sp. CS131 on R5A.
Figure 6
Figure 6
Upset Plot from the compounds detected via GS-MS from the assay confronting Streptomyces sp. CS147 and Escovopsis weberi. Ew: volatiles produced by E. weberi; SFMc: volatile produced during the coculture of E. weberi–Streptomyces CS147 on soy flour mannitol (SFM) medium; SFM147: volatiles produced by CS147 on SFM; R5A147: volatiles produced by CS147 on R5A medium; R5Ac: volatiles produced during the coculture of E. weberi–Streptomyces sp. CS147 on R5A.
Figure 7
Figure 7
Upset Plot from the compounds detected via GS-MS from the assay confronting Streptomyces sp. CS014 and Escovopsis weberi. Ew: volatiles produced by E. weberi; SFMc: volatile produced during the coculture of E. weberi–Streptomyces sp. CS014 on soy flour mannitol (SFM) medium; SFM14: volatiles produced by CS014 on SFM; R5A14: volatiles produced by CS014 on R5A medium; R5Ac: volatiles produced during the coculture E. weberi–Streptomyces sp. CS014 on R5A.
Figure 8
Figure 8
Phytophthora cinnamomi plates when cocultured in volatile organic compound (VOC) chambers against Streptomyces spp. CS014, CS57, CS065a, CS081a, CS090a, CS113 (first row), CS131, CS147, CS149, CS159, CS207, and CS227 (second row). The last image corresponds to the control of the assay (a VOC chamber without a Streptomyces sp. culture).
Figure 9
Figure 9
Sclerotinia spp. plates when cocultured in VOC (volatile organic compound) chambers against Streptomyces sp. CS014, CS57, CS065a, CS081a, CS090a, CS113 (first row), CS131, CS147, CS149, CS159, CS207, and CS227 (second row). The last image corresponds to the control of the assay (a VOC chamber without a Streptomyces sp. culture).
Figure 10
Figure 10
Reduction in Escovopsis weberi growth via multiple cocultures of different Streptomyces sp. strains. From left to right, E. weberi when cultured alone; E. weberi cultured in the presence of strain CS081a; E. weberi cultured in the presence of strain CS090a; E. weberi cultured in the presence of strains CS081a and CS090a.
Figure 11
Figure 11
Potato Dextrose Agar (PDA) + phenol red plates in VOC (volatile organic compound) chambers in the presence of Streptomyces spp. First row corresponds to plates cocultured with Streptomyces spp.; second row corresponds to plates cocultured with Streptomyces spp. and Escovopsis weberi.
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