Skip to main content

Metabolite profiles of interacting mycelial fronts differ for pairings of the wood decay basidiomycete fungus, Stereum hirsutum with its competitors Coprinus micaceus and Coprinus disseminatus

Abstract

The paper presents the first proof-of principle study of metabolite profiles of the interacting mycelial fronts of a wood decomposer basidiomycete, Stereum hirsutum, paired with two competitor basidiomycetes, Coprinus disseminatus and C. micaceus, using TLC and GC-TOF-MS profiling. GC-TOF-MS profiles were information rich, with a total of 190 metabolite peaks detected and more than 120 metabolite peaks detected per sample. The metabolite profiles were able to discriminate between the interactions of S. hirsutum with the two species of Coprinus. In confrontation with C. micaceus, where S. hirsutum mycelial fronts always overgrew those of C. micaceus, there were down-regulations of metabolites in the interaction zone, compared to monocultures of both S. hirsutum and C. micaceus. In contrast, in pairings with C. disseminatus, whose mycelia overgrew those of S. hirsutum, there were some up-regulations compared with monoculture controls, the majority of the metabolites being characteristic of the S. hirsutum monoculture profile. These differences indicate that up-regulation of metabolites in the mycelia of S. hirsutum may be connected to a defensive role or to stress. The results also show proof of principle for the employment of metabolic profiling for biological discovery studies of metabolites produced by fungi that could be applied to natural product screening programmes.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abdi, H. (2007). Bonferroni and Sidak corrections for multiple comparisons. In N. J. Salkind (Ed.), Encyclopedia of measurement and statistics. Thousand Oaks: Sage.

    Google Scholar 

  • Bilski, P., Li, M. Y., Ehrenshaft, M., Daub, M. E., & Chignell, C. F. (2000). Vitamin B-6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants. Photochemistry and Photobiology, 71, 129–134.

    PubMed  Article  CAS  Google Scholar 

  • Boddy, L. (2000). Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiology Ecology, 31, 185–194.

    PubMed  Article  CAS  Google Scholar 

  • Boddy, L., & Rayner, A. D. M. (1983). Ecological roles of basidiomycetes forming decay communities in attached oak branches. New Phytologist, 93, 77–88.

    Article  Google Scholar 

  • Bourbonnais, R., Paice, M. G., Reid, I. D., Lanthier, P., & Yaguchi, M. (1995). Lignin oxidation by laccase isozymes from trametes-versicolor and role of the mediator 2,2′-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymerization. Applied and Environmental Microbiology, 61, 1876–1880.

    PubMed  CAS  Google Scholar 

  • Collin, H. A. (2001). Secondary product formation in plant tissue cultures. Plant Growth Regulation, 34, 119–134.

    Article  CAS  Google Scholar 

  • Gloer, J. B. (1995). The chemistry of fungal antagonism and defense. Canadian Journal of Botany-Revue Canadienne De Botanique, 73, S1265–S1274.

    CAS  Article  Google Scholar 

  • Gregorio, A. P. F., Da Silva, I. R., Sedarati, M. R., & Hedger, J. N. (2006). Changes in production of lignin degrading enzymes during interactions between mycelia of the tropical decomposer basidiomycetes Marasmiellus troyanus and Marasmius pallescens. Mycological Research, 110, 161–168.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Han, Y. S., Van der Heijden, R., & Verpoorte, R. (2001). Biosynthesis of anthraquinones in cell cultures of the Rubiaceae. Plant Cell Tissue and Organ Culture, 67, 201–220.

    Article  CAS  Google Scholar 

  • Hedger, J. N. (1985). Tropical agarics: Resource relations and fruiting periodicity. In D. Moore, L. A. Casselton, D. A. Wood, & J. C. Frankland (Eds.), Developmental biology of higher fungi (pp. 41–86). Cambridge: Cambridge University Press.

    Google Scholar 

  • Heilmann-Clausen, J., & Boddy, L. (2005). Inhibition and stimulation effects in communities of wood decay fungi: Exudates from colonized wood influence growth by other species. Microbial Ecology, 49, 399–406.

    PubMed  Article  CAS  Google Scholar 

  • Humphris, S. N., Wheatley, R. E., & Bruce, A. (2001). The effects of specific volatile organic compounds produced by Trichoderma spp. on the growth of wood decay basidiomycetes. Holzforschung, 55, 233–237.

    Article  CAS  Google Scholar 

  • Hynes, J., Muller, C. T., Jones, T. H., & Boddy, L. (2007). Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. Journal of Chemical Ecology, 33, 43–57.

    PubMed  Article  CAS  Google Scholar 

  • Ikediugwu, F. E. O., & Webster, J. (1970). Hyphal interference in a range of coprophilous fungi. Transactions of the British Mycological Society, 54, 205–210.

    Article  Google Scholar 

  • Johannes, C., & Majcherczyk, A. (2000). Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Applied and Environmental Microbiology, 66, 524–528.

    PubMed  Article  CAS  Google Scholar 

  • Joliffe, I. T. (1986). Principal components analysis. New York: Springer-Verlag.

    Google Scholar 

  • Kruskal, W. H., & Wallis, W. A. (1952). Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association, 47, 583–621.

    Article  Google Scholar 

  • Magnenot, M. F. (1952). Recherches methodiques sur les champignons de certains bois en decomposition. Revue Generale de Botanique, 59, 381–401.

    Google Scholar 

  • Magnuson, J. K., & Lasure, L. L. (2004). Organic acid production by filamentous fungi. In J. Lange & L. Lange (Eds.), Advance in fungal biotechnology for industry, agriculture and medicine (pp. 307–340). Washington: Kluwer Academic/Plenum Publishers.

    Google Scholar 

  • O’Hagan, S., Dunn, W. B., Brown, M., Knowles, J. D., & Kell, D. B. (2005). Closed-loop, multiobjective optimization of analytical instrumentation: Gas chromatography/time-of-flight mass spectrometry of the metabolomes of human serum and of yeast fermentations. Analytical Chemistry, 77, 290–303.

    PubMed  Article  CAS  Google Scholar 

  • Rayner, A. D. M., & Boddy, L. (1988). Fungal decomposition of wood, its biology and ecology. New York: John Wiley.

    Google Scholar 

  • Rayner, A. D. M., Griffith, G. S., & Ainsworth, A. M. (1994). Mycelial interconnectedness. In N. A. R. Gow & G. M. Gadd (Eds.), The growing fungus (pp. 21–40). London: Chapman and Hall.

    Chapter  Google Scholar 

  • Score, A. J., Palfreyman, J. W., & White, N. A. (1997). Extracellular phenoloxidase and peroxidase enzyme production during interspecific fungal interactions. International Biodeterioration & Biodegradation, 39, 225–233.

    Article  CAS  Google Scholar 

  • Shearer, C. A. (1995). Fungal competition. Canadian Journal of Botany-Revue Canadienne De Botanique, 73, S1259–S1264.

    Google Scholar 

  • Sung, B. K., Kim, M. K., Lee, W. H., Lee, D. H., & Lee, H. S. (2004). Growth responses of Cassia obtusifolia toward human intestinal bacteria. Fitoterapia, 75, 505–509.

    PubMed  Article  CAS  Google Scholar 

  • Tanaka, T., Tateno, Y., & Gojobori, T. (2005). Evolution of vitamin B-6 (pyridoxine) metabolism by gain and loss of genes. Molecular Biology and Evolution, 22, 243–250.

    PubMed  Article  CAS  Google Scholar 

  • Wheatley, R. E. (2002). The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81, 357–364.

    Article  CAS  Google Scholar 

  • White, N. A., & Boddy, L. (1992). Extracellular enzyme localization during interspecific fungal interactions. FEMS Microbiology Letters, 98, 75–79.

    Article  CAS  Google Scholar 

  • Williams, E. N. D., Todd, N. K., & Rayner, A. D. M. (1981). Spatial development of populations of Coriolus versicolor. New Phytologist, 89, 307–319.

    Article  Google Scholar 

  • Wold, H. (1966). Estimation of principal components and related models by iterative least squares. In P. R. Krishnaiah (Ed.), Multivariate analysis (pp. 391–420). New York: Academic Press.

    Google Scholar 

Download references

Acknowledgement

This work was financially supported by University of Westminster, Cavendish Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Diluka Peiris.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Peiris, D., Dunn, W.B., Brown, M. et al. Metabolite profiles of interacting mycelial fronts differ for pairings of the wood decay basidiomycete fungus, Stereum hirsutum with its competitors Coprinus micaceus and Coprinus disseminatus . Metabolomics 4, 52–62 (2008). https://doi.org/10.1007/s11306-007-0100-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11306-007-0100-4

Keywords

  • Metabolite profiling
  • Basidiomycete fungi
  • Mycelial interactions