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Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal

Becher, Paul G. LU ; Verschut, Vasiliki ; Bibb, Maureen J. ; Bush, Matthew J. ; Molnár, Béla P. ; Barane, Elisabeth LU ; Al-Bassam, Mahmoud M. ; Chandra, Govind ; Song, Lijiang and Challis, Gregory L. , et al. (2020) In Nature Microbiology
Abstract

Volatile compounds emitted by bacteria are often sensed by other organisms as odours, but their ecological roles are poorly understood1,2. Well-known examples are the soil-smelling terpenoids geosmin and 2-methylisoborneol (2-MIB)3,4, which humans and various animals sense at extremely low concentrations5,6. The conservation of geosmin biosynthesis genes among virtually all species of Streptomyces bacteria (and genes for the biosynthesis of 2-MIB in about 50%)7,8, suggests that the volatiles provide a selective advantage for these soil microbes. We show, in the present study, that these volatiles mediate interactions of apparent mutual benefit between streptomycetes and springtails... (More)

Volatile compounds emitted by bacteria are often sensed by other organisms as odours, but their ecological roles are poorly understood1,2. Well-known examples are the soil-smelling terpenoids geosmin and 2-methylisoborneol (2-MIB)3,4, which humans and various animals sense at extremely low concentrations5,6. The conservation of geosmin biosynthesis genes among virtually all species of Streptomyces bacteria (and genes for the biosynthesis of 2-MIB in about 50%)7,8, suggests that the volatiles provide a selective advantage for these soil microbes. We show, in the present study, that these volatiles mediate interactions of apparent mutual benefit between streptomycetes and springtails (Collembola). In field experiments, springtails were attracted to odours emitted by Streptomyces colonies. Geosmin and 2-MIB in these odours induce electrophysiological responses in the antennae of the model springtail Folsomia candida, which is also attracted to both compounds. Moreover, the genes for geosmin and 2-MIB synthases are under the direct control of sporulation-specific transcription factors, constraining emission of the odorants to sporulating colonies. F. candida feeds on the Streptomyces colonies and disseminates spores both via faecal pellets and through adherence to its hydrophobic cuticle. The results indicate that geosmin and 2-MIB production is an integral part of the sporulation process, completing the Streptomyces life cycle by facilitating dispersal of spores by soil arthropods.

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Nature Microbiology
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  • pmid:32251369
  • scopus:85083270255
ISSN
2058-5276
DOI
10.1038/s41564-020-0697-x
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English
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06d3c07f-583b-4ae8-af14-33e10337a6f8
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2020-05-08 16:35:58
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@article{06d3c07f-583b-4ae8-af14-33e10337a6f8,
  abstract     = {<p>Volatile compounds emitted by bacteria are often sensed by other organisms as odours, but their ecological roles are poorly understood<sup>1,2</sup>. Well-known examples are the soil-smelling terpenoids geosmin and 2-methylisoborneol (2-MIB)<sup>3,4</sup>, which humans and various animals sense at extremely low concentrations<sup>5,6</sup>. The conservation of geosmin biosynthesis genes among virtually all species of Streptomyces bacteria (and genes for the biosynthesis of 2-MIB in about 50%)<sup>7,8</sup>, suggests that the volatiles provide a selective advantage for these soil microbes. We show, in the present study, that these volatiles mediate interactions of apparent mutual benefit between streptomycetes and springtails (Collembola). In field experiments, springtails were attracted to odours emitted by Streptomyces colonies. Geosmin and 2-MIB in these odours induce electrophysiological responses in the antennae of the model springtail Folsomia candida, which is also attracted to both compounds. Moreover, the genes for geosmin and 2-MIB synthases are under the direct control of sporulation-specific transcription factors, constraining emission of the odorants to sporulating colonies. F. candida feeds on the Streptomyces colonies and disseminates spores both via faecal pellets and through adherence to its hydrophobic cuticle. The results indicate that geosmin and 2-MIB production is an integral part of the sporulation process, completing the Streptomyces life cycle by facilitating dispersal of spores by soil arthropods.</p>},
  author       = {Becher, Paul G. and Verschut, Vasiliki and Bibb, Maureen J. and Bush, Matthew J. and Molnár, Béla P. and Barane, Elisabeth and Al-Bassam, Mahmoud M. and Chandra, Govind and Song, Lijiang and Challis, Gregory L. and Buttner, Mark J. and Flärdh, Klas},
  issn         = {2058-5276},
  language     = {eng},
  month        = {04},
  publisher    = {Springer Nature},
  series       = {Nature Microbiology},
  title        = {Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal},
  url          = {http://dx.doi.org/10.1038/s41564-020-0697-x},
  doi          = {10.1038/s41564-020-0697-x},
  year         = {2020},
}