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Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris

Nature Biotechnology volume 29, pages 922–927 (2011)Cite this article

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Abstract

Thermostable enzymes and thermophilic cell factories may afford economic advantages in the production of many chemicals and biomass-based fuels. Here we describe and compare the genomes of two thermophilic fungi, Myceliophthora thermophila and Thielavia terrestris. To our knowledge, these genomes are the first described for thermophilic eukaryotes and the first complete telomere-to-telomere genomes for filamentous fungi. Genome analyses and experimental data suggest that both thermophiles are capable of hydrolyzing all major polysaccharides found in biomass. Examination of transcriptome data and secreted proteins suggests that the two fungi use shared approaches in the hydrolysis of cellulose and xylan but distinct mechanisms in pectin degradation. Characterization of the biomass-hydrolyzing activity of recombinant enzymes suggests that these organisms are highly efficient in biomass decomposition at both moderate and high temperatures. Furthermore, we present evidence suggesting that aside from representing a potential reservoir of thermostable enzymes, thermophilic fungi are amenable to manipulation using classical and molecular genetics.

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Figure 1: Genome organization of M. thermophila and T. terrestris.
Figure 2: Analysis of transcription profiles.
Figure 3: Release of reducing sugars from alfalfa straw by crude extracellular enzymes from thermophilic and nonthermophilic fungi.

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Gene Expression Omnibus

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Acknowledgements

The genome sequencing and analysis were conducted by the US Department of Energy Joint Genome Institute and supported by the Office of Science of the US Department of Energy under contract no. DE-AC02-05CH11231. The work on transcriptomes, enzyme characterization and the Myceliophthora exo-proteome was supported by the Cellulosic Biofuel Network of the Agriculture Bioproducts Innovation Program of Agriculture and Agri-Food Canada, Genome Canada and Genome Québec.

Author information

Author notes

  1. Diego Martinez

    Present address: Present address: Broad Institute of MIT & Harvard, Cambridge, Massachusetts USA.,

  2. Randy M Berka, Igor V Grigoriev and Adrian Tsang: These authors contributed equally to this work.

Authors and Affiliations

  1. Novozymes, Inc., Davis, California, USA

    Randy M Berka, Paul Harris, Mark Wogulis, Alfredo Lopez de Leon & Michael W Rey

  2. US Department of Energy Joint Genome Institute, Walnut Creek, California, USA

    Igor V Grigoriev, Robert Otillar, Asaf Salamov, Erika Lindquist & Susan Lucas

  3. HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, USA

    Jane Grimwood & Jeremy Schmutz

  4. Centre for Structural and Functional Genomics, Concordia University, Montreal, Quebec, Canada

    Ian Reid, Nadeeza Ishmael, Tricia John, Corinne Darmond, Marie-Claude Moisan, Justin Powlowski, Annie Bellemare, David Taylor, Gregory Butler, Sophia Ushinsky, Reginald Storms & Adrian Tsang

  5. Architecture et Fonction des Macromolécules Biologiques, CNRS/Universités de Provence/Université de la Mediterranée, Marseille, France

    Bernard Henrissat, Pedro M Coutinho & Vincent Lombard

  6. Department of Biology, University of New Mexico, Albuquerque, New Mexico, USA

    Donald O Natvig & Diego Martinez

  7. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands

    Ronald P de Vries, Iris E Allijn & Joost van den Brink

  8. Microbiology and Kluyver Centre for Genomics of Industrial Fermentation, Utrecht University, Utrecht, The Netherlands

    Ronald P de Vries

  9. Sandia National Laboratory, Albuquerque, New Mexico, USA

    Amy J Powell

  10. Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, Australia

    Ian T Paulsen & Liam D H Elbourne

  11. Fungal Biotechnology Team, Pacific Northwest National Laboratory, Richland, Washington, USA

    Scott E Baker & Jon Magnuson

  12. McGill University and Génome Québec Innovation Centre, Montreal, Canada

    Sylvie LaBoissiere

  13. University of Glasgow, Glasgow, UK

    A John Clutterbuck

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  1. Randy M Berka
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Contributions

The final text of the manuscript was written by R.M.B. and A.T., and reviewed by I.V.G.; who together also coordinated the overall analysis. I.V.G. coordinated both genome projects at the Joint Genome Institute. R.M.B. prepared the genomic DNA of T. terrestris and T.J. the DNA of M. thermophila. A.T. coordinated the transcriptome and exo-proteome work, and analyzed the transcriptomes. S.L. and E.L. led genome and cDNA sequencing. J.G. and J.S. finished and assembled both genomes. R.O. and A.S. annotated and analyzed the genomes, synteny and GC content. I.R. processed the RNA-Seq data and analyzed the cell wall proteins. N.I. coordinated the sample preparation for transcriptome analysis and analyzed the lignocellulolytic proteins. B.H., P.M.C. and V.L. performed the comparative analysis of the carbohydrate-active proteins. C.D. conducted the enzymatic hydrolysis of straws and M.-C.M. prepared the samples for transcriptome and exo-proteome analysis. D.O.N. analyzed the mating types and phylogeny of thermophilic fungi. E.L. coordinated the cDNA synthesis and EST analysis. A.B. coordinated the cloning and expression of xylanase genes. D.T. characterized the biochemical properties of the xylanases. R.P. de V., I.E.A, and J. van den B. examined the growth on different substrates. P.H. analyzed the GH61 proteins and J.P. membrane biogenesis. G.B. analyzed the secretomes. S.U. and R.S. analyzed the chromatin structure and dynamics. A.J.P. examined melanin pigment biogenesis. I.T.P. and L.D.H.E. analyzed transporters. S.E.B. analyzed secondary metabolism. J.M. examined oxidative stress. M.W. reviewed proteases and peptidases. S.L. examined the exo-proteomes. A.J.C. looked for repeat-induced polymorphisms. D.M. contributed computational tools for viewing T. terrestris transcriptome data. A.L.de L. and M.W.R. examined oxidoreductases and chitinases, respectively.

Corresponding author

Correspondence to Adrian Tsang.

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Berka, R., Grigoriev, I., Otillar, R. et al. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 29, 922–927 (2011). https://doi.org/10.1038/nbt.1976

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