Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

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

Nature Microbiology volume 5, pages 821–829 (2020)Cite this article

Subjects

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 (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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Attraction of springtails to Streptomyces headspace, geosmin or 2-MIB.
Fig. 2: Antennal responses to Streptomyces headspace components in F. candida.
Fig. 3: Developmental regulation of geosmin and 2-MIB biosynthetic genes.
Fig. 4: Dispersal of S. coelicolor spores mediated by springtails.

Similar content being viewed by others

Data availability

The transcriptional profiling data from Affymetrix arrays and the ChIP–seq data in Fig. 3 have been deposited at the ArrayExpress Archive of Functional Genomics Data (http://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-5853 for the whiH mutant array data, E-MTAB-2716 for the bldM mutant array data, E-MTAB-6702 for the WhiH ChIP–seq data and E-MTAB-2698 for the BldM ChIP–seq data). Source data for Figs. 1a,b,e,f,g and 4b,c and Extended Data Figs. 1a,b,c, 4, 5 and 6a,b,c are included in this letter and its Supplementary Information files. Other data that support the findings of the present study are available from the corresponding authors upon reasonable request.

References

  1. Audrain, B., Farag, M. A., Ryu, C. M. & Ghigo, J. M. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol. Rev. 39, 222–233 (2015).

    Article  CAS  PubMed  Google Scholar 

  2. Tyc, O., Song, C., Dickschat, J. S., Vos, M. & Garbeva, P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 25, 280–292 (2017).

    Article  CAS  PubMed  Google Scholar 

  3. Cane, D. E. & Ikeda, H. Exploration and mining of the bacterial terpenome. Acc. Chem. Res. 45, 463–472 (2012).

    Article  CAS  PubMed  Google Scholar 

  4. Jiang, J., He, X. & Cane, D. E. Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat. Chem. Biol. 3, 711–715 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Liato, V. & Aider, M. Geosmin as a source of the earthy-musty smell in fruits, vegetables and water: origins, impact on foods and water, and review of the removing techniques. Chemosphere 181, 9–18 (2017).

    Article  CAS  PubMed  Google Scholar 

  6. Stensmyr, M. C. et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345–1357 (2012).

    Article  CAS  PubMed  Google Scholar 

  7. Rabe, P., Citron, C. A. & Dickschat, J. S. Volatile terpenes from actinomycetes: a biosynthetic study correlating chemical analyses to genome data. ChemBioChem 14, 2345–2354 (2013).

    Article  CAS  PubMed  Google Scholar 

  8. Yamada, Y. et al. Terpene synthases are widely distributed in bacteria. Proc. Natl Acad. Sci. USA 112, 857–862 (2015).

    Article  CAS  PubMed  Google Scholar 

  9. Gerber, N. N. & Lechevalier, H. A. Geosmin, an earthly-smelling substance isolated from actinomycetes. Appl. Microbiol. 13, 935–938 (1965).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Barka, E. A. et al. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 80, 1–43 (2016).

    Article  PubMed  Google Scholar 

  11. Jones, S. E. et al. Streptomyces exploration is triggered by fungal interactions and volatile signals. eLife 6, e21738 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bush, M. J., Tschowri, N., Schlimpert, S., Flärdh, K. & Buttner, M. J. c-di-GMP signalling and the regulation of developmental transitions in streptomycetes. Nat. Rev. Microbiol. 13, 749–760 (2015).

    Article  CAS  PubMed  Google Scholar 

  13. Becher, P. G., Bengtsson, M., Hansson, B. S. & Witzgall, P. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J. Chem. Ecol. 36, 599–607 (2010).

    Article  CAS  PubMed  Google Scholar 

  14. Melo, N. et al. Geosmin attracts Aedes aegypti mosquitoes to oviposition sites. Curr. Biol. 30, 127–134 (2020).

    Article  PubMed  CAS  Google Scholar 

  15. Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).

    Article  CAS  PubMed  Google Scholar 

  16. Bengtsson, G., Erlandsson, A. & Rundgren, S. Fungal odour attracts soil collembola. Soil Biol. Biochem. 20, 25–30 (1988).

    Article  Google Scholar 

  17. Thimm, T., Hoffmann, A., Borkott, H., Munch, J. C. & Tebbe, C. C. The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Appl. Environ. Microbiol. 64, 2660–2669 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kaur, T., Vasudev, A., Sohal, S. K. & Manhas, R. K. Insecticidal and growth inhibitory potential of Streptomyces hydrogenans DH16 on major pest of India, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). BMC Microbiol. 14, 227 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Tran, A. et al. C. elegans avoids toxin-producing Streptomyces using a seven transmembrane domain chemosensory receptor. eLife 6, e23770 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Al-Bassam, M. M., Bibb, M. J., Bush, M. J., Chandra, G. & Buttner, M. J. Response regulator heterodimer formation controls a key stage in Streptomyces development. PLoS Genet. 10, e1004554 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Saito, N., Matsubara, K., Watanabe, M., Kato, F. & Ochi, K. Genetic and biochemical characterization of EshA, a protein that forms large multimers and affects developmental processes in Streptomyces griseus. J. Biol. Chem. 278, 5902–5911 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Persson, J., Chater, K. F. & Flärdh, K. Molecular and cytological analysis of the expression of Streptomyces sporulation regulatory gene whiH. FEMS Microbiol. Lett. 341, 96–105 (2013).

    Article  CAS  PubMed  Google Scholar 

  23. Ryding, N. J. et al. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 29, 343–357 (1998).

    Article  CAS  PubMed  Google Scholar 

  24. Gallagher, K. A. et al. c-di-GMP arms an anti-sigma to control progression of multicellular differentiation in Streptomyces. Mol. Cell 77, 586–599 (2019).

    Article  PubMed  CAS  Google Scholar 

  25. Bentley, R. & Meganathan, R. Geosmin and methylisoborneol biosynthesis in streptomycetes. Evidence for an isoprenoid pathway and its absence in non-differentiating isolates. FEBS Lett. 125, 220–222 (1981).

    Article  CAS  PubMed  Google Scholar 

  26. Schöller, C. E., Gurtler, H., Pedersen, R., Molin, S. & Wilkins, K. Volatile metabolites from actinomycetes. J. Agric. Food Chem. 50, 2615–2621 (2002).

    Article  PubMed  CAS  Google Scholar 

  27. Ghiradella, H. & Radigan, W. Collembolan cuticle: wax layer and anti-wetting properties. J. Insect Physiol. 20, 301–306 (1974).

    Article  CAS  PubMed  Google Scholar 

  28. Helbig, R., Nickerl, J., Neinhuis, C. & Werner, C. Smart skin patterns protect springtails. PLoS ONE 6, e25105 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ruddick, S. M. & Williams, S. T. Studies on the ecology of actinomycetes in soil. V. Some factors influencing the dispersal and adsorption of spores in soil. Soil Biol. Biochem. 4, 93–103 (1972).

    Article  Google Scholar 

  30. Jørgensen, H. B., Elmholt, S. & Petersen, H. Collembolan dietary specialisation on soil grown fungi. Biol. Fertil. Soils 39, 9–15 (2003).

    Article  Google Scholar 

  31. Staaden, S., Milcu, A., Rohlfs, M. & Scheu, S. Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour. Soil Biol. Biochem. 43, 1411–1416 (2011).

    Article  CAS  Google Scholar 

  32. Faddeeva-Vakhrusheva, A. et al. Gene family evolution reflects adaptation to soil environmental stressors in the genome of the collembolan Orchesella cincta. Genome Biol. Evol. 8, 2106–2117 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Faddeeva-Vakhrusheva, A. et al. Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genom. 18, 493 (2017).

    Article  CAS  Google Scholar 

  34. Böllmann, J., Elmer, M., Wöllecke, J., Raidl, S. & Hüttl, R. F. Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiologia 53, 107–114 (2010).

    Article  Google Scholar 

  35. Rohlfs, M. & Churchill, A. C. L. Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet. Biol. 48, 23–34 (2011).

    Article  CAS  PubMed  Google Scholar 

  36. Höckelmann, C., Becher, P. G., Von Reuß, S. H. & Jüttner, F. Sesquiterpenes of the geosmin-producing cyanobacterium Calothrix PCC 7507 and their toxicity to invertebrates. Z. Naturforsch. C 64, 49–55 (2009).

    Article  PubMed  Google Scholar 

  37. Booth, R. G. & Anderson, J. M. The influence of fungal food quality on the growth and fecundity of Folsomia candida (Collembola: Isotomidae). Oecologia 38, 317–323 (1979).

    Article  CAS  PubMed  Google Scholar 

  38. Kaltenpoth, M., Göttler, W., Herzner, G. & Strohm, E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15, 475–479 (2005).

    Article  CAS  PubMed  Google Scholar 

  39. Chater, K. F. & Chandra, G. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30, 651–672 (2006).

    Article  CAS  PubMed  Google Scholar 

  40. Getahun, M. N. et al. Intracellular regulation of the insect chemoreceptor complex impacts odour localization in flying insects. J. Exp. Biol. 219, 3428–3438 (2016).

    Article  PubMed  Google Scholar 

  41. Missbach, C. et al. Evolution of insect olfactory receptors. eLife 3, e02115 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Vos, M., Wolf, A. B., Jennings, S. J. & Kowalchuk, G. A. Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol. Rev. 37, 936–954 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Holighaus, G. & Rohlfs, M. Volatile and non-volatile fungal oxylipins in fungus-invertebrate interactions. Fungal Ecol. 38, 28–36 (2019).

    Article  Google Scholar 

  44. Datsenko, K. A. & Wanner, B. W. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Gust, B., Challis, G. L., Fowler, K., Kieser, T. & Chater, K. F. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl Acad. Sci. USA 100, 1541–1546 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gust, B. et al. Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv. Appl. Microbiol. 54, 107–128 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. Practical Streptomyces Genetics (The John Innes Foundation, 2000).

  48. Bush, M. J., Bibb, M. J., Chandra, G., Findlay, K. C. & Buttner, M. J. Genes required for aerial growth, cell division, and chromosome segregation are targets of WhiA before sporulation in Streptomyces venezuelae. mBio 4, e00684–00613 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Lindén, A. & Mäntyniemi, S. Using the negative binomial distribution to model overdispersion in ecological count data. Ecology 92, 1414–1421 (2011).

    Article  PubMed  Google Scholar 

  50. Holmstrup, M. et al. Physiological and molecular responses of springtails exposed to phenanthrene and drought. Environ. Poll. 184, 370–376 (2014).

    Article  CAS  Google Scholar 

  51. Agger, S. A., Lopez-Gallego, F., Hoye, T. R. & Schmidt-Dannert, C. Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. J. Bacteriol. 190, 6084–6096 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Andreadis, S. S., Cloonan, K. R., Myrick, A. J., Chen, H. & Baker, T. C. Isolation of a female-emitted sex pheromone component of the fungus gnat, Lycoriella ingenua, attractive to males. J. Chem. Ecol. 41, 1127–1136 (2015).

    Article  CAS  PubMed  Google Scholar 

  53. Citron, C. A., Barra, L., Wink, J. & Dickschat, J. S. Volatiles from nineteen recently genome sequenced actinomycetes. Org. Biomol. Chem. 13, 2673–2683 (2015).

    Article  CAS  PubMed  Google Scholar 

  54. He, X. & Cane, D. E. Mechanism and stereochemistry of the germacradienol/germacrene D synthase of Streptomyces coelicolor A3(2). J. Am. Chem. Soc. 126, 2678–2679 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. Beadle, G. W. & Ephrussi, B. The differentiation of eye pigments in Drosophila as studied by transplantation. Genetics 21, 225–247 (1936).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Bengtsson, G., Hedlund, K. & Rundgren, S. Selective odour perception in the soil collembola Onychiurus armatus. J. Chem. Ecol. 17, 2113–2125 (1991).

    Article  CAS  PubMed  Google Scholar 

  57. Kaplan, E. L. & Meier, P. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53, 457–481 (1958).

    Article  Google Scholar 

  58. Bibb, M. J., Domonkos, A., Chandra, G. & Buttner, M. J. Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by σBldN and a cognate anti-sigma factor, RsbN. Mol. Microbiol. 84, 1033–1049 (2012).

    Article  CAS  PubMed  Google Scholar 

  59. Hesketh, A., Kock, H., Mootien, S. & Bibb, M. The role of absC, a novel regulatory gene for secondary metabolism, in zinc-dependent antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 74, 1427–1444 (2009).

    Article  CAS  PubMed  Google Scholar 

  60. Dromph, K. M. Dispersal of entomopathogenic fungi by collembolans. Soil Biol. Biochem. 33, 2047–2051 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank O. Gustafsson for assistance with electron microscopy, M. Holmstrup for helping us to establish F. candida, M. Karlsson for confirming species identity of F. candida, T. Verschut for discussions, G. Birgersson for technical support (statistics@slu) and F. Jüttner for comments on the manuscript. This work was funded by a PlantLink seed money grant to P.G.B. and K.F., BBSRC grants (nos. BB/H006125/1 and BB/I002197/1) to M.J. Buttner, BBSRC Institute Strategic Programme grants (nos. BB/J004561/1 and BB/P012523/1) to the John Innes Centre, grants from the Crafoord Foundation and support through the SLU Centre for Biological Control to P.G.B., and grants from the Swedish Research Council (grant nos. 2010-4463 and 2015-05452) to K.F. B.P.M. was supported by the New National Excellence Program of the Ministry of Human Capacities (ÚNKP-19-4) and the János Bolyai Research Scholarship of the Hungarian Academy of Sciences.

Author information

Authors and Affiliations

  1. Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden

    Paul G. Becher, Vasiliki Verschut & Béla P. Molnár

  2. Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, Norwich, UK

    Maureen J. Bibb, Matthew J. Bush, Mahmoud M. Al-Bassam, Govind Chandra & Mark J. Buttner

  3. Zoology Department, Plant Protection Institute, Centre for Agricultural Research, Budapest, Hungary

    Béla P. Molnár

  4. Department of Biology, Lund University, Lund, Sweden

    Elisabeth Barane & Klas Flärdh

  5. Department of Chemistry, University of Warwick, Coventry, UK

    Lijiang Song & Gregory L. Challis

  6. Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia

    Gregory L. Challis

Authors
  1. Paul G. Becher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vasiliki Verschut
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maureen J. Bibb
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthew J. Bush
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Béla P. Molnár
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elisabeth Barane
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mahmoud M. Al-Bassam
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Govind Chandra
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lijiang Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gregory L. Challis
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mark J. Buttner
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Klas Flärdh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.J. Buttner, P.G.B. and K.F. designed the research. V.V. performed the field trap experiments and statistical analyses. V.V. and P.G.B. did the work involving springtails and analyses of volatiles; together with E.B. and K.F. they performed the spore dispersal assays. B.P.M. performed the GC–EAD experiments. M.J. Bibb and M.M.A.-B. performed the time-resolved transcriptional profiling, M.J. Bibb, M.J. Bush and M.M.A.-B. performed the ChIP–seq experiments. G.C. analysed the ChIP–seq data. M.J. Bibb and M.J. Bush constructed mutants and plasmids. E.B. and K.F. identified WhiH as a regulator of geoA. L.S. and G.L.C. performed initial GC–MS analyses of the Streptomyces mutants. P.G.B. and K.F. wrote the manuscript together with V.V. and M.J. Buttner. All the authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Paul G. Becher or Klas Flärdh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Effects and production of volatiles from Streptomyces coelicolor.

Captures of insects (a) and arachnids (b) on the ground of a field site using sticky traps baited with Streptomyces coelicolor cultured on agar medium, compared to control traps that were kept without bait or held a fresh, non-inoculated plate of agar culture medium (n=19). The boxplots show the medians, lower- and upper quartiles as well as the span of data points that are within 1.5 times the interquartile range. Electroantennographic responses (c) towards 2-MIB or geosmin puffed into an air stream passing over antennae of the springtails Folsomia candida. The average responses to all tested stimuli (n=8 per stimulus) significantly differed from the antennal response to charcoal filtered air. Statistical difference is labelled by different letters above the columns; error bars show the standard errors (X25, 48 =629.54, P<0.001). GC-MS chromatograms (d) of S. coelicolor wild type and two biosynthetic mutants show that geosmin or geosmin and 2-MIB, respectively, are missing from the geoA and geoA mibAB mutants (strains J3003 and J2192, respectively). The headspace collection for the specific strains was repeated three times with similar results.

Source data

Extended Data Fig. 2

Absolute amounts (ng) of geosmin and 2-methylisoborneol (2-MIB) tested as individual compounds or as components of Streptomyces headspace in the Y-tube choice assay.

Extended Data Fig. 3 Folsomia candida springtails feed on Streptomyces coelicolor mycelium.

(a) Folsomia candida springtails feeding on sporulating Streptomyces coelicolor. The bacteria were grown as lawns on agar covered with cellophane membranes, and then scraped off and transferred to F. candida kept on a Petri dish lined with gypsum plaster. The photo shows the dark bacterial biomass visible inside the guts of the animals as well as faecal pellets covering the plaster. (b, c) Agar plugs with developed colonies of S. coelicolor strain M145 were placed in containers with autoclaved potting soil, either without springtails (b), or with 10 F. candida individuals (c). After 6 days of incubation, the colonies in soil without springtails remained intact, while the colonies in soil with springtails were consumed by grazing of the animals. Control experiments showed that the animals did not graze on uninoculated agarose plugs (not shown). Scale bars, 10 mm. Similar observations were made in three independent experiments. In addition to the grazing, the ability of springtails to disperse S. coelicolor was clearly reflected in the large number of microcolonies (seen as white spots in the photographs) developing throughout the microcosms containing F. candida individuals.

Extended Data Fig. 4 Folsomia candida springtails are positively affected by being fed Streptomyces coelicolor mycelium.

Survival, moulting and oviposition of female F. candida kept for 10 days on sporulating cultures of S. coelicolor (n=31, grey solid lines) or SFM agar controls (n=23, light grey dashed lines). Survival on S. coelicolor was as high as on SFM control (a, X21, 54 =1.7, P=0.195). Exposure to S. coelicolor had a positive effect on the initiation of moulting (b, X21, 54 =11, P<0.001***) and oviposition (c, X21, 54 =6.4, P=0.011*) with more eggs being laid (d, X21, 54 =6.064, P=0.0138*; the boxplot shows the medians, lower- and upper quartiles as well as the span of data points that are within 1.5 times the interquartile range).

Source data

Extended Data Fig. 5 Effects of developmental regulatory genes bldM and whiH on production of geosmin and 2-methylisoborneol (2-MIB) in Streptomyces venezuelae.

(a) Gas chromatograms analysed for the presence of 2-MIB, geosmin and germacrene D in Streptomyces venezuelae headspace sampled from wild-type, whiH, bldM mutants or a system control. The chromatograms and the quantification of Streptomyces metabolites (b; n=3; error bars give the standard deviation of the mean) illustrate that in comparison to wild-type, geosmin and germacrene D were reduced in the whiH mutant. None of the three Streptomyces metabolites was detected (n.d.) in the bldM mutant or the control. C12 –C14 hydrocarbons were used for calculation of retention indices. Octyl acetate was introduced with the internal standard heptyl acetate (not shown), which was used for quantification.

Source data

Extended Data Fig. 6 Assays of spore adherence and dispersal.

To compare dispersal of sporulating and non-sporulating strains, individuals of F. candida (n=12) were fed for 3 days with developed mycelium of S. coelicolor strain M145 or its congenic non-sporulating whiG mutant J2400. CFUs that could be washed off (0.05% Tween-20) from individual animals were quantified by plating on SFM agar. Significantly more spores than hyphae had adhered to the springtail body (a, two-tailed Mann Whitney test, P<0.001 **). To monitor the release of viable cells by defaecation, each washed springtail was allowed to roam for 20 h on MM agar before colonies were allowed to develop. Significantly more CFU were excreted from springtails that had been feeding on the sporulating Streptomyces strain (b, two-tailed Mann Whitney test, P<0.001 **). The boxplots show the medians, lower- and upper quartiles as well as the span of data points (smallest to largest). In a dispersal assay (c), S. coelicolor strains J2192/pIJ10646 (geoA mibAB mutant with geoA and mibAB genes provided in trans on integrated plasmid) and J2192/pIJ10770 (geoA mibAB mutant with empty vector) were allowed to develop and sporulate (5 days) in small spots in center of MM agar plates. Two springtails (F. candida) (n=13) were released for 2 h on each plate. Animals were then removed, plates incubated, and Streptomyces colonies counted. The presence of geoA and mibAB genes (strain J2192/pIJ10646) resulted in significantly more CFU being dispersed by springtails (c, two-tailed Mann Whitney test, P=0.022 *). Error bars show the standard error of the mean. Volatiles from cultures of these strains were collected for 24 h on an air filter, eluted with hexane, and analysed by GC-MS. Chromatograms (d) show that geosmin and 2-MIB were present in strain J2192/pIJ10646 but not detectable (n.d.) in the non-complemented J2192/pIJ10770 strain. The analyses were independently repeated three times with similar results.

Source data

Supplementary information

Supplementary Information

Supplementary Discussion, Table 1 and references.

Reporting Summary

Supplementary Video

QuickTime video showing springtails (F. candida) feeding on S. coelicolor biomass. The S. coelicolor strain M145 was grown on SFM agar medium covered with a cellophane membrane to allow abundant sporulation (8 d, 27 °C), scraped off from the plate, and placed on a Petri dish lined with gypsum plaster on which springtails were kept. Similar observations were made in three independent experiments.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 4

Statistical source data.

Source Data Extended Data Fig. 1

Statistical source data.

Source Data Extended Data Fig. 4

Statistical source data.

Source Data Extended Data Fig. 5

Statistical source data.

Source Data Extended Data Fig. 6

Statistical source data.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Becher, P.G., Verschut, V., Bibb, M.J. et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat Microbiol 5, 821–829 (2020). https://doi.org/10.1038/s41564-020-0697-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41564-020-0697-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing