Skip to main content
Log in

Transcriptome analysis of differential gene expression in Dichomitus squalens during interspecific mycelial interactions and the potential link with laccase induction

  • Microbial Genetics, Genomics and Molecular Biology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Interspecific mycelial interactions between white rot fungi are always accompanied by an increased production of laccase. In this study, the potential of the white rot fungus Dichomitus squalens to enhance laccase production during interactions with two other white rot fungi, Trametes versicolor or Pleurotus ostreatus, was assessed. To probe the mechanism of laccase induction and the role that laccase plays during combative interaction, we analyzed the differential gene expression profile of the laccase induction response to stressful conditions during fungal interaction. We further confirmed the expression patterns of 16 selected genes by qRT-PCR analysis. We noted that many differentially expressed genes (DEGs) encoded proteins that were involved in xenobiotic detoxification and reactive oxygen species (ROS) generation or reduction, including aldo/keto reductase, glutathione S-transferases, cytochrome P450 enzymes, alcohol oxidases and dehydrogenase, manganese peroxidase and laccase. Furthermore, many DEG-encoded proteins were involved in antagonistic mechanisms of nutrient acquisition and antifungal properties, including glycoside hydrolase, glucanase, chitinase and terpenoid synthases. DEG analyses effectively revealed that laccase induction was likely caused by protective responses to oxidative stress and nutrient competition during interspecific fungal interactions.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arfi, Y., Levasseur, A., and Record, E. 2013. Differential gene expression in Pycnoporus coccineus during interspecific mycelial interactions with different competitors. Appl. Environ. Microbiol. 79, 6626–6636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aust, S.D., Swaner, P.R., and Stahl, J.D. 2004. Detoxification and metabolism of chemicals by white-rot fungi, pp. 3–14. In Pesticide decontamination and detoxification. Oxford University Press, Washington, D.C., USA.

    Google Scholar 

  • Aust, S.D., Swaner, P.R., Stahl, J.D., Gan, J.J., Zhu, P.C., Aust, S.D., and Lemley, A.T. 2004. Detoxification and metabolism of chemicals by white-rot fungi. Acs. Symposium 863, 3–14.

    Article  CAS  Google Scholar 

  • Baldrian, P. 2004. Increase of laccase activity during interspecific interactions of white-rot fungi. FEMS Microbiol. Ecol. 50, 245–253.

    Article  CAS  PubMed  Google Scholar 

  • Boddy, L. 2000. Interspecific combative interactions between wooddecaying basidiomycetes. FEMS Microbiol. Ecol. 31, 185–194.

    Article  CAS  PubMed  Google Scholar 

  • Chen, C.H., Ferreira, J.C.B., Gross, E.R., and Mochly-Rosen, D. 2014. Targeting aldehyde dehydrogenase 2: new therapeutic opportunities. Physiol. Rev. 94, 1–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi, Y., Hatakka, A., and Maijala, P. 2007. Can co-culturing of two white-rot fungi increase lignin degradation and the production of lignin-degrading enzymes? Int. Biodeterior. Biodegradation 59, 32–39.

    Article  CAS  Google Scholar 

  • Cho, N.S., Wilkolazka, A.J., Staszczak, M., Cho, H.Y., and Ohga, S. 2009. The role of laccase from white rot fungi to stress conditions. J. Fac. Agr. Kyushu Univ. 54, 81–83.

    CAS  Google Scholar 

  • Cruz-Ortega, R., Lara-Núñez, A., and Anaya, A.L. 2007. Allelochemical stress can trigger oxidative damage in receptor plants. Plant Signal. Behav. 2, 269–270.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daniel, G., Volc, J., Filonova, L., Plihal, O., Kubatova, E., and Halada, P. 2007. Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood. Appl. Environ. Microbiol. 73, 6241–6253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, Y.C., Wang, W., Hu, Z.C., Fu, M.L., and Chen, Q.H. 2012. The synergistic effect on production of lignin-modifying enzymes through submerged co-cultivation of Phlebia radiata, Dichomitus squalens and Ceriporiopsis subvermispora using agricultural residues. Bioprocess Biosyst. Eng. 35, 751–760.

    Article  CAS  PubMed  Google Scholar 

  • Eggert, C., Temp, U., and Eriksson, K.E. 1996. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl. Environ. Microbiol. 62, 1151.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenman, H.C. and Casadevall, A. 2012. Synthesis and assembly of fungal melanin. Appl. Microbiol. Biotechnol. 93, 931–940.

    Article  CAS  PubMed  Google Scholar 

  • Eisenman, H.C., Mues, M., Weber, S.E., Frases, S., Chaskes, S., Gerfen, G., and Casadevall, A. 2007. Cryptococcus neoformans laccase catalyses melanin synthesis from both D- and L-DOPA. Microbiology 153, 3954–3962.

    Article  CAS  PubMed  Google Scholar 

  • El Ariebi, N., Hiscox, J., Scriven, S.A., Müller, C.T., and Boddy, L. 2016. Production and effects of volatile organic compounds during interspecific interactions. Fungal Ecol. 20, 144–154.

    Article  Google Scholar 

  • Evans, J.A., Eyre, C.A., Rogers, H.J., Boddy, L., and Müller, C.T. 2008. Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media. Fungal Ecol. 1, 57–68.

    Article  Google Scholar 

  • Eyre, C., Muftah, W., Hiscox, J., Hunt, J., Kille, P., Boddy, L., and Rogers, H.J. 2010. Microarray analysis of differential gene expression elicited in Trametes versicolor during interspecific mycelial interactions. Fungal Biol. 114, 646–660.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira Gregorio, A.P., Da Silva, I.R., Sedarati, M.R., and 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. Mycol. Res. 110, 161–168.

    Article  CAS  PubMed  Google Scholar 

  • Flores, C., Vidal, C., Trejo-Hernandez, M.R., Galindo, E., and Serrano-Carreon, L. 2009. Selection of Trichoderma strains capable of increasing laccase production by Pleurotus ostreatus and Agaricus bisporus in dual cultures. J. Appl. Microbiol. 106, 249–257.

    Article  CAS  PubMed  Google Scholar 

  • Floudas, D., Binder, M., Riley, R., Barry, K., Blanchette, R.A., Henrissat, B., Martínez, A.T., Otillar, R., Spatafora, J.W., and Yadav, J.S. 2012. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715.

    Article  CAS  PubMed  Google Scholar 

  • Flundas, D. and Hibbett, D.S. 2012. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715.

    Article  CAS  Google Scholar 

  • Garcia-Sanchez, M., Garrido, I., Casimiro Ide, J., Casero, P.J., Espinosa, F., Garcia-Romera, I., and Aranda, E. 2012. Defence response of tomato seedlings to oxidative stress induced by phenolic compounds from dry olive mill residue. Chemosphere 89, 708–716.

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez, F.J. 2005. Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat. Res. 569, 101–110.

    Article  CAS  PubMed  Google Scholar 

  • Heilmann-Clausen, J. and Boddy, L. 2005. Inhibition and stimulation effects in communities of wood decay fungi: exudates from colonized wood influence growth by other species. Microb. Ecol. 49, 399–406.

    Article  CAS  PubMed  Google Scholar 

  • Hiscox, J., Baldrian, P., Rogers, H.J., and Boddy, L. 2010. Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor. Fungal Genet. Biol. 47, 562–571.

    Article  CAS  PubMed  Google Scholar 

  • Iakovlev, A., Olson, A., Elfstrand, M., and Stenlid, J. 2004. Differential gene expression during interactions between Heterobasidion annosum and Physisporinus sanguinolentus. FEMS Microbiol. Lett. 241, 79–85.

    Article  CAS  PubMed  Google Scholar 

  • Jaszek, M., Grzywnowicz, K., Malarczyk, E., and Leonowicz, A. 2006. Enhanced extracellular laccase activity as a part of the response system of white rot fungi: Trametes versicolor and Abortiporus biennis to paraquat-caused oxidative stress conditions. Pestic. Biochem. Physiol. 85, 147–154.

    Article  CAS  Google Scholar 

  • Jeon, J.R., Baldrian, P., Murugesan, K., and Chang, Y.S. 2012. Laccase-catalysed oxidations of naturally occurring phenols: from in vivo biosynthetic pathways to green synthetic applications. Microb. Biotechnol. 5, 318–332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonkers, W., Rodriguez Estrada, A.E., Lee, K., Breakspear, A., May, G., and Kistler, H.C. 2012. Metabolome and transcriptome of the interaction between Ustilago maydis and Fusarium verticillioides in vitro. Appl. Environ. Microbiol. 78, 3656–3667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kannaiyan, R., Mahinpey, N., Kostenko, V., and Martinuzzi, R.J. 2015. Nutrient media optimization for simultaneous enhancement of the laccase and peroxidases production by coculture of Dichomitus squalens and Ceriporiopsis subvermispora. Biotechnol. Appl. Biochem. 62, 173–185.

    Article  CAS  PubMed  Google Scholar 

  • Kuhar, F., Castiglia, V., and Levin, L. 2015. Enhancement of laccase production and malachite green decolorization by co-culturing Ganoderma lucidum and Trametes versicolor in solid-state fermentation. Int. Biodeterior. Biodegradation 104, 238–243.

    Article  CAS  Google Scholar 

  • Lara, O.T., Riveros, R.H., and Aguirre, J. 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. Microbiol. 50, 1241–1255.

    Article  CAS  Google Scholar 

  • Li, Q., Bai, Z., O’Donnell, A., Harvey, L.M., Hoskisson, P.A., and McNeil, B. 2011. Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol. Lett. 33, 457–467.

    Article  CAS  PubMed  Google Scholar 

  • Li, B. and Dewey, C.N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak, K.J. and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Mariani, D., Mathias, C.J., da Silva, C.G., Herdeiro Rda, S., Pereira, R., Panek, A.D., Eleutherio, E.C., and Pereira, M.D. 2008. Involvement of glutathione transferases, Gtt1and Gtt2, with oxidative stress response generated by H2O2 during growth of Saccharomyces cerevisiae. Redox Rep. 13, 246–254.

    Article  CAS  PubMed  Google Scholar 

  • Mayer, A.M. and Staples, R.C. 2002. Laccase: new functions for an old enzyme. Phytochemistry 60, 551–565.

    Article  CAS  PubMed  Google Scholar 

  • Mazhawidza, W., Banda, Y., and Rajendran, N. 2014. Bioinformatic identification of aldo-keto reductase from newly isolated arthrobacter nicotianae strain PR and its phylogenetic analysis among soil bacteria. Open Access J. Sci. Technol. 2, 1–7.

    Article  CAS  Google Scholar 

  • Nosanchuk, J.D. and Casadevall, A. 2003. The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5, 203–223.

    Article  CAS  PubMed  Google Scholar 

  • Peiris, D., Dunn, W., Brown, M., Kell, D., Roy, I., and Hedger, J. 2008. 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.

    Article  CAS  Google Scholar 

  • Piscitelli, A., Giardina, P., Lettera, V., Pezzella, C., Sannia, G., and Faraco, V. 2011. Induction and transcriptional regulation of laccases in fungi. Curr. Genomics 12, 104–112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riva, S. 2006. Laccases: blue enzymes for green chemistry. Trends Biotechnol. 24, 219–226.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, M.D., McCarthy, D.J., and Smyth, G.K. 2010. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.

    Article  CAS  PubMed  Google Scholar 

  • Shetty, N.P., Mehrabi, R., Lutken, H., Haldrup, A., Kema, G.H., Collinge, D.B., and Jorgensen, H.J. 2007. Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol. 174, 637–647.

    Article  CAS  PubMed  Google Scholar 

  • Silar, P. 2005. Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant. Mycol. Res. 109, 137–149.

    Article  CAS  PubMed  Google Scholar 

  • Ujor, V.C., Monti, M., Peiris, D.G., Clements, M.O., and Hedger, J.N. 2012. The mycelial response of the white-rot fungus, Schizophyllum commune to the biocontrol agent, Trichoderma viride. Fungal Biol. 116, 332–341.

    Article  PubMed  Google Scholar 

  • Wei, F., Hong, Y., Liu, J., Yuan, J., Fang, W., Peng, H., and Xiao, Y. 2010. Gongronella sp. induces overproduction of laccase in Panus rudis. J. Basic Microbiol. 50, 98–103.

    Article  CAS  PubMed  Google Scholar 

  • Wells, J.M. and Boddy, L. 2002. Interspecific carbon exchange and cost of interactions between basidiomycete mycelia in soil and wood. Funct. Ecol. 16, 153–161.

    Article  Google Scholar 

  • Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C.Y., and Wei, L. 2011. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316–322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Y., Fan, F., Zhuo, R., Ma, F., Gong, Y., Wan, X., Jiang, M., and Zhang, X. 2012. Expression of the laccase gene from a white rot fungus in Pichia pastoris can enhance the resistance of this yeast to H2O2-mediated oxidative stress by stimulating the glutathionebased antioxidative system. Appl. Environ. Microbiol. 78, 5845–5854.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, X. and Williamson, P.R. 2004. Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res. 5, 1–10.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Feng Luo.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhong, Z., Li, N., He, B. et al. Transcriptome analysis of differential gene expression in Dichomitus squalens during interspecific mycelial interactions and the potential link with laccase induction. J Microbiol. 57, 127–137 (2019). https://doi.org/10.1007/s12275-019-8398-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-019-8398-y

Keywords

Navigation