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Open Access Research article

The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown

Anthony Levasseur12*, Anne Lomascolo12, Olivier Chabrol3, Francisco J Ruiz-Dueñas4, Eva Boukhris-Uzan5, François Piumi12, Ursula Kües6, Arthur F J Ram7, Claude Murat8, Mireille Haon12, Isabelle Benoit9, Yonathan Arfi10, Didier Chevret11, Elodie Drula1213, Min Jin Kwon7, Philippe Gouret3, Laurence Lesage-Meessen12, Vincent Lombard1213, Jérôme Mariette14, Céline Noirot14, Joohae Park7, Aleksandrina Patyshakuliyeva9, Jean Claude Sigoillot12, Ad Wiebenga9, Han A B Wösten15, Francis Martin8, Pedro M Coutinho1213, Ronald P de Vries9, Angel T Martínez4, Christophe Klopp14, Pierre Pontarotti3, Bernard Henrissat1213 and Eric Record12

Author Affiliations

1 INRA, UMR1163 Biotechnologie des Champignons Filamenteux, Aix-Marseille Université, Polytech Marseille, 163 avenue de Luminy, CP 925, 13288 Marseille Cedex 09, France

2 Aix-Marseille Université, INRA, UMR1163 Biotechnologie des Champignons Filamenteux, Faculté des Sciences de Luminy-Polytech, CP 925, 13288 Marseille Cedex 09, France

3 Aix-Marseille Université, CNRS, Centrale Marseille, I2M, UMR7373, FR 4213 - FR Eccorev 3098, équipe EBM, 13331 Marseille, France

4 Centro de Investigaciones Biológicas (CIB), CSIC, Ramiro de Maeztu 9, E-28040 Madrid, Spain

5 CNRS ISM2 UMR 7353, Aix-Marseille Université, Campus Scientifique de Saint Jérôme avenue Escadrille Normandie-Niemen, case 341, 13397 Marseille Cedex 20, France

6 Molecular Wood Biotechnology and Technical Mycology, Büsgen-Instit ute, Georg-August-University, 37077 Göttingen, Germany

7 Department of Molecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands

8 INRA, UMR 1136 INRA Université de Lorraine ‘Interactions Arbres-Microorganismes’, Labex ARBRE, FR EFABA, 54280 Champenoux, France

9 Fungal Physiology, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands

10 The Weizmann Institute of Science, Faculty of Biological Chemistry, 234 Herzl Street, Rehovot 7610001, Israël

11 INRA, UMR1319 Micalis, Plateforme d’Analyse Protéomique de Paris Sud-Ouest, 78352 Jouy-en-Josas, France

12 Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, 13288 Marseille, France

13 Centre National de la Recherche Scientifique, CNRS UMR 7257, 13288 Marseille, France

14 Plateforme bioinformatique Genotoul, UR875 Biométrie et Intelligence Artificielle, INRA, 31326 Castanet-Tolosan, France

15 Department of Microbiology, Kluyver Centre for Genomics of Industrial Fermentation – Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands

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BMC Genomics 2014, 15:486  doi:10.1186/1471-2164-15-486

Published: 18 June 2014

Abstract

Background

Saprophytic filamentous fungi are ubiquitous micro-organisms that play an essential role in photosynthetic carbon recycling. The wood-decayer Pycnoporus cinnabarinus is a model fungus for the study of plant cell wall decomposition and is used for a number of applications in green and white biotechnology.

Results

The 33.6 megabase genome of P. cinnabarinus was sequenced and assembled, and the 10,442 predicted genes were functionally annotated using a phylogenomic procedure. In-depth analyses were carried out for the numerous enzyme families involved in lignocellulosic biomass breakdown, for protein secretion and glycosylation pathways, and for mating type. The P. cinnabarinus genome sequence revealed a consistent repertoire of genes shared with wood-decaying basidiomycetes. P. cinnabarinus is thus fully equipped with the classical families involved in cellulose and hemicellulose degradation, whereas its pectinolytic repertoire appears relatively limited. In addition, P. cinnabarinus possesses a complete versatile enzymatic arsenal for lignin breakdown. We identified several genes encoding members of the three ligninolytic peroxidase types, namely lignin peroxidase, manganese peroxidase and versatile peroxidase. Comparative genome analyses were performed in fungi displaying different nutritional strategies (white-rot and brown-rot modes of decay). P. cinnabarinus presents a typical distribution of all the specific families found in the white-rot life style. Growth profiling of P. cinnabarinus was performed on 35 carbon sources including simple and complex substrates to study substrate utilization and preferences. P. cinnabarinus grew faster on crude plant substrates than on pure, mono- or polysaccharide substrates. Finally, proteomic analyses were conducted from liquid and solid-state fermentation to analyze the composition of the secretomes corresponding to growth on different substrates. The distribution of lignocellulolytic enzymes in the secretomes was strongly dependent on growth conditions, especially for lytic polysaccharide mono-oxygenases.

Conclusions

With its available genome sequence, P. cinnabarinus is now an outstanding model system for the study of the enzyme machinery involved in the degradation or transformation of lignocellulosic biomass.

Keywords:
Pycnoporus cinnabarinus; Genome annotation; CAZy; Auxiliary activities; Oxidoreductase; White-rot fungi; Lignocellulose