Skip to main content
SpringerLink
Log in

Changes in Volatile Production During the Course of Fungal Mycelial Interactions Between Hypholoma fasciculare and Resinicium bicolor

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The mycelia of two wood decay basidiomycete fungi were grown opposing each other across a 1-μm pore membrane supported on the surface of malt broth, contained within a sealable reaction vessel. Production of volatiles during the time course of interaction was followed by collecting head space samples by solid phase microextraction (100 μm polydimethylsiloxane fiber) on five occasions over 25 d following coinoculation of the fungi: 1, 3 (i.e., immediately prior to mycelial contact), 9 (1–2 d after initiation of pigment production by Resinicium bicolor), 17, and 25 d. Ten volatiles were produced during interactions that were not detected in single species controls. In general, most (18) fungal volatiles were sesquiterpenes eluted between 12.5 and 21 min, with a further two eluted at 29.1 and 33.9 min; a benzoic acid methyl ester, a benzyl alcohol, and a quinolinium type compound with a distinctive fragmentation pattern at m/z 203, 204, 206, and 207 were also identified; three volatiles with m/z maxima of 163, 159, and 206–208, respectively, remained unidentified. The results are discussed in relation to possible ecological roles of volatiles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abraham, W. R. 2001. Bioactive sesquiterpenes produced by fungi: Are they useful for humans as well? Curr. Med. Chem. 8:583–606.

    PubMed  CAS  Google Scholar 

  • Boddy, L. 2000. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol. 31:185–194.

    Article  PubMed  CAS  Google Scholar 

  • Boddy, L. 2001. Fungal community ecology and wood decomposition processes in angiosperms: From standing tree to complete decay of coarse woody debris. Ecol. Bull. 49:43–56.

    Google Scholar 

  • Bulow, N. and König, W. A. 2000. The role of germacrene D as a precursor in sesquiterpene biosynthesis: Investigations of acid catalyzed, photochemically and thermally induced rearrangements. Phytochemistry 55:141–168.

    Article  PubMed  CAS  Google Scholar 

  • Cakir, A., Kordali, S., Kilic, H., and Kaya, E. 2005. Antifungal properties of essential oil and crude extracts of Hypericum linarioides Bosse. Biochem. Syst. Ecol. 33:245–256.

    Article  CAS  Google Scholar 

  • Cheng, S. S., Lin, H. Y., and Chang, S. T. 2005. Chemical composition and antifungal activity of essential oils from different tissues of Japanese cedar (Cryptomeria japonica). J. Agric. Food Chem. 53:614–619.

    Article  PubMed  CAS  Google Scholar 

  • De Lacy Costello, B. P. J., Evans, P., Ewen, R. J., Gunson, H. E., Jones, P. R. H., Ratcliffe, N. M., and Spencer-Phillips, P. T. N. 2001. Gas chromatography–mass spectrometry analysis of volatile organic compounds from potato tubers inoculated with Phytophthora infestans or Fusarium coeruleum. Plant Pathol. 50:489–496.

    Article  Google Scholar 

  • Demyttenaere, J. C. R., Morina, R. M., De Kimpe, N., and Sandra, P. 2004. Use of headspace solid-phase microextraction and headspace sorptive extraction for the detection of the volatile metabolites produced by toxigenic Fusarium species. J. Chromatogr. A 1027:147–154.

    Article  PubMed  CAS  Google Scholar 

  • El-Sayed, A. M. 2005. The pherobase: Database of insect pheromones and semiochemicals. <http://www.pherobase.net>. Accessed: November 2005.

  • Ewen, R. J., Jones, P. R. H., Ratcliffe, N. M., and Spencer-Phillips, P. T. N. 2004. Identification by gas chromatography–mass spectrometry of the volatile organic compounds emitted from the wood-rotting fungi Serpula lacrymans and Coniophora puteana, and from Pinus sylvestris timber. Mycol. Res. 108:806–814.

    Article  PubMed  CAS  Google Scholar 

  • Fäldt, J., Jonsell, M., Nordlander, G., and Borg-Karlson, A. K. 1999. Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J. Chem. Ecol. 25:567–590.

    Article  Google Scholar 

  • Florianowicz, T. 2000. Inhibition of growth and sporulation of Penicillium expansum by extracts of selected basidiomycetes. Acta Soc. Botanicorum Pol. 69:263–267.

    Google Scholar 

  • Geervliet, J. B. F., Posthumus, M. A., Vet, L. E. M., and Dicke, M. 1997. Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23:2935–2954.

    CAS  Google Scholar 

  • Griffith, G. S., Rayner, A. D. M., and Wildman, H. G. 1994a. Extracellular metabolites and mycelial morphogenesis of Hypholoma fasciculare and Phlebia radiata (Hymenomycetes). Nova Hedwigia 59:311–329.

    Google Scholar 

  • Griffith, G. S., Rayner, A. D. M., and Wildman, H. G. 1994b. Interspecific interactions and mycelial morphogenesis of Hypholoma fasciculare (Agaricaceae). Nova Hedwigia 59:47–75.

    Google Scholar 

  • Griffith, G. S., Rayner, A. D. M., and Wildman, H. G. 1994c. Interspecific interactions, mycelial morphogenesis and extracellular metabolite production in Phlebia radiata (Aphyllophorales). Nova Hedwigia 59:331–344.

    Google Scholar 

  • Hartlieb, E. and Rembold, H. 1996. Behavioral response of female Helicoverpa (Heliothis) armigera Hb (Lepidoptera: Noctuidae) moths to synthetic pigeonpea (Cajanus cajan L) kairomone. J. Chem. Ecol. 22:821–837.

    Article  CAS  Google Scholar 

  • Heilmann-Clausen, J. and Boddy, L. 2005. Inhibition and stimulation effects in communities of wood decay fungi: Exudates from colonised wood influence growth by other species. Microb. Ecol. 49:1–8.

    Article  Google Scholar 

  • Humphris, S. N., Bruce, A., Buultjens, E., and Wheatley, R. E. 2002. The effects of volatile microbial secondary metabolites on protein synthesis in Serpula lacrymans. FEMS Microbiol. Lett. 210:215–219.

    Article  PubMed  CAS  Google Scholar 

  • Jeleń, H. H. 2003. Use of solid phase microextraction (SPME) for profiling fungal volatile metabolites. Lett. Appl. Microbiol. 36:263–267.

    Article  PubMed  Google Scholar 

  • Kahlos, K., Kiviranta, J. L. J., and Hiltunen, R. V. K. 1994. Volatile constituents of wild and in vitro cultivated Gloeophyllum odoratum. Phytochemistry 36:917–922.

    Article  PubMed  CAS  Google Scholar 

  • Kirby, J. J. H., Stenlid, J., and Holdenrieder, O. 1990. Population-structure and responses to disturbance of the basidiomycete Resinicium bicolor. Oecologia 85:178–184.

    Article  Google Scholar 

  • Korpi, A., Pasanen, A. L. and Viitanen, H. 1999. Volatile metabolites of Serpula lacrymans, Coniophora puteana, Poria placenta, Stachybotrys chartarum and Chaetomium globosum. Build. Environ. 34:205–211.

    Article  Google Scholar 

  • Mozuraitis, R., Stranden, M., Ramirez, M. I., Borg-Karlson, A. K., and Mustaparta, H. 2002. (−)-Germacrene D increases attraction and oviposition by the tobacco budworm moth Heliothis virescens. Chem. Senses 27:505–509.

    Article  PubMed  CAS  Google Scholar 

  • Nilsson, T., Larsen, T. O., Montanarella, L., and Madsen, J. O. 1996. Application of head-space solid-phase microextraction for the analysis of volatile metabolites emitted by Penicillium species. J. Microbiol. Methods 25:245–255.

    Article  CAS  Google Scholar 

  • Prosser, I., Altug, I. G., Phillips, A. L., Konig, W. A., Bouwmeester, H. J., and Beale, M. H. 2004. Enantiospecific (+)- and (−)-germacrene D synthases, cloned from goldenrod, reveal a functionally active variant of the universal isoprenoid-biosynthesis aspartate-rich motif. Arch. Biochem. Biophys. 432:136–144.

    Article  PubMed  CAS  Google Scholar 

  • Rayner, A. D. M. and Boddy, L. 1988. Fungal Decomposition of Wood: Its Biology and Ecology. Wiley, New York.

    Google Scholar 

  • Rayner, A. D. M., Griffith, G. S., and Wildman, H. G. 1994. Induction of metabolic and morphogenetic changes during mycelial interactions among species of higher fungi. Biochem. Soc. Trans. 22:389–394.

    PubMed  CAS  Google Scholar 

  • Rösecke, J. and König, W. A. 2000. Constituents of various wood-rotting basidiomycetes. Phytochemistry 54:603–610.

    Article  PubMed  Google Scholar 

  • Rösecke, J., Pietsch, M., and König, W. A. 2000. Volatile constituents of wood-rotting basidiomycetes. Phytochemistry 54:747–750.

    Article  PubMed  Google Scholar 

  • Røstelien, T., Borg-Karlson, A. K., Faldt, J., Jacobsson, U., and Mustaparta, H. 2000. The plant sesquiterpene germacrene D specifically activates a major type of antennal receptor neuron of the tobacco budworm moth Heliothis virescens. Chem. Senses 25:141–148.

    Article  PubMed  Google Scholar 

  • Roy, G., Laflamme, G., Bussieres, G., and Dessureault, M. 2003. Field tests on biological control of Heterobasidion annosum by Phaeotheca dimorphospora in comparison with Phlebiopsis gigantea. For. Pathol. 33:127–140.

    Google Scholar 

  • Savoie, J. M. 2001. Variability in brown line formation and extracellular laccase production during interaction between white-rot basidiomycetes and Trichoderma harzianum biotype th2. Mycologia 93:243–248.

    Article  CAS  Google Scholar 

  • Schoeman, M. W., Webber, J. F., and Dickinson, D. J. 1996. The effect of diffusible metabolites of Trichoderma harzianum on in vitro interactions between basidiomycete isolates at two different temperature regimes. Mycol. Res. 100:1454–1458.

    Article  CAS  Google Scholar 

  • Score, A. J., Palfreyman, J. W., and White, N. A. 1997. Extracellular phenoloxidase and peroxidase enzyme production during interspecific fungal interactions. Int. Biodeterior. Biodegrad. 39:225–233.

    Article  CAS  Google Scholar 

  • Stadler, M. and Sterner, O. 1998. Production of bioactive secondary metabolites in the fruit bodies of macrofungi as a response to injury. Phytochemistry 49:1013–1019.

    Article  CAS  Google Scholar 

  • Sunesson, A. L., Vaes, W. H. J., Nilsson, C. A., Blomquist, G., Andersson, B., and Carlson, R. 1995. Identification of volatile metabolites from 5 fungal species cultivated on 2 media. Appl. Environ. Microbiol. 61:2911–2918.

    PubMed  CAS  Google Scholar 

  • Viiri, H., Annila, E., Kitunen, V., and Niemela, P. 2001. Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees-Struct. Funct. 15:112–122.

    CAS  Google Scholar 

  • Wald, P., Crockatt, M., Gray, V., and Boddy, L. 2004a. Growth and interspecific interactions of the rare oak polypore Piptoporus quercinus. Mycol. Res. 108:189–197.

    Article  PubMed  Google Scholar 

  • Wald, P., Pitkanen, S., and Boddy, L. 2004b. Interspecific interactions between the rare tooth fungi Creolophus cirrhatus, Hericium erinaceus and H coralloides and other wood decay species in agar and wood. Mycol. Res. 108:1447–1457.

    Article  PubMed  Google Scholar 

  • Wang, S. Y., Wu, C. L., Chug, F. H., Chien, S. C., Kuo, Y. H., Shyur, L. F., and Chang, S. T. 2005. Chemical composition and antifungal activity of essential oil isolated from Chamaecyparis formosensis Matsum. Wood. Holzforschung 59:295–299.

    Article  CAS  Google Scholar 

  • Wheatley, R., Hackett, C., Bruce, A., and Kundzewicz, A. 1997. Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. Inhibitory to wood decay fungi. Int. Biodeterior. Biodegrad. 39:199–205.

    Article  CAS  Google Scholar 

  • Wheatley, R. E. 2002. The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364.

    Article  PubMed  CAS  Google Scholar 

  • White, N. A. and Boddy, L. 1992. Extracellular enzyme localization during interspecific fungal interactions. FEMS Microbiol. Lett. 98:75–79.

    Article  CAS  Google Scholar 

  • Wiens, J. A., Cates, R. G., Rotenberry, J. T., Cobb, N., Vanhorne, B., and Redak, R. A. 1991. Arthropod dynamics on sagebrush (Artemisia tridentata)—effects of plant chemistry and avian predation. Ecol. Monogr. 61:299–321.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Natural Environment Research Council for funding (003/00731), John Hedger, the Cardiff University Fungal Ecology Group, and Tim Rotheray for discussion and for Fig. 1.

Author information

Authors and Affiliations

  1. Cardiff School of Biosciences, Cardiff University, Cardiff, CF10 3TL, UK

    Juliet Hynes, Carsten T. Müller, T. Hefin Jones & Lynne Boddy

Authors
  1. Juliet Hynes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carsten T. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Hefin Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lynne Boddy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lynne Boddy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hynes, J., Müller, C.T., Jones, T.H. et al. Changes in Volatile Production During the Course of Fungal Mycelial Interactions Between Hypholoma fasciculare and Resinicium bicolor . J Chem Ecol 33, 43–57 (2007). https://doi.org/10.1007/s10886-006-9209-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9209-6

Keywords

Search

Navigation