Abstract

Wood biomass is the most abundant feedstock envisioned for the development of modern biorefineries. However, the cost-effective conversion of this form of biomass into commodity products is limited by its resistance to enzymatic degradation. Here we describe a new family of fungal lytic polysaccharide monooxygenases (LPMOs) prevalent among white-rot and brown-rot basidiomycetes that is active on xylans—a recalcitrant polysaccharide abundant in wood biomass. Two AA14 LPMO members from the white-rot fungus Pycnoporus coccineus substantially increase the efficiency of wood saccharification through oxidative cleavage of highly refractory xylan-coated cellulose fibers. The discovery of this unique enzyme activity advances our knowledge on the degradation of woody biomass in nature and offers an innovative solution for improving enzyme cocktails for biorefinery applications.

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GenBank/EMBL/DDBJ

Protein Data Bank

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Acknowledgements

We thank the European Synchrotron Radiation Facility (Grenoble), and the synchrotron Soleil (Gif-sur-Yvette) for beamtime allocation and assistance. We thank S. Tapin (Centre Technique du Papier, France) for providing cellulose fibers, E. Bonnin and J. Vigouroux for compositional analyses, G. Toriz and P. Gatenholm (Chalmers University of Technology, Sweden) for providing purified wood xylan, L. Foucat and X. Falourd for their valued assistance with treatments of the NMR data, E. Perrin for the excellent technical support for TEM images, B. Seantier for the access and assistance to AFM facilities, D. Hartmann and E. Bertrand for their help with enzyme production in bioreactor, D. Gillet (Mahtani Chitosan, India) for providing chitin, and D. Navarro and G. Anasontzis for insightful discussions. M.C. was funded by a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Program (328162). S.L., M.-N.R. and J.-G.B. were funded by the Microbio-E A*MIDEX project (ANR-11-IDEX-0001-02). This work was supported in part by the CNRS and the French Infrastructure for Integrated Structural Biology (FRISBI) ANR-10-INSB-05-01. N.L. and B.H. were supported by Agence Française de l'Environnement et de la Maîtrise de l'Energie (1201C102). P.H.W., G.J.D. and L.C. thank the UK Biotechnology and Biological Sciences Research Council (BB/L001926/1 and BB/L021633/1) for funding. G.J.D. is the Royal Society Ken Murray Research Professor.

Author information

Author notes

    • Marie Couturier
    •  & Simon Ladevèze

    These authors contributed equally to this work.

Affiliations

  1. INRA, Aix Marseille University, Biodiversité et Biotechnologie Fongiques (BBF), Marseille, France.

    • Marie Couturier
    • , Simon Ladevèze
    • , Kristian E Frandsen
    • , Aurore Labourel
    • , Isabelle Herpoël-Gimbert
    • , Sacha Grisel
    • , Mireille Haon
    • , Marie-Noëlle Rosso
    •  & Jean-Guy Berrin
  2. Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix-Marseille University, Marseille, France.

    • Gerlind Sulzenbacher
    • , Nicolas Lenfant
    •  & Bernard Henrissat
  3. INRA, USC1408 Architecture et Fonction des Macromolécules Biologiques (AFMB), Marseille, France.

    • Gerlind Sulzenbacher
    •  & Bernard Henrissat
  4. Department of Chemistry, University of York, York, UK.

    • Luisa Ciano
    • , Gideon J Davies
    •  & Paul H Walton
  5. INRA, Unité de Recherche Biopolymères Interactions Assemblages (BIA), Nantes, France.

    • Mathieu Fanuel
    • , Céline Moreau
    • , Ana Villares
    • , Bernard Cathala
    • , Hélène Rogniaux
    •  & David Ropartz
  6. IMBE Aix Marseille University, IRD CNRS UAPV, Faculté de Pharmacie, Marseille, France.

    • Florence Chaspoul
  7. Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.

    • Bernard Henrissat

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Contributions

M.C. identified the new enzymes and performed biochemical characterization. M.-N.R. was in charge of transcriptomic and proteomic analyses. M.C., S.L., S.G., I.H.-G. and M.H. performed production of proteins in flasks and bioreactors. F.C. performed ICP-MS analysis. S.L. and S.G. performed synergy assays with xylanase and protein crystallization. S.L. and G.S. solved the crystal structure of PcAA14B. B.H. and N.L. performed bioinformatic analyses. M.C., S.L., S.G. performed HPAEC analyses. M.F., D.R. and H.R. identified oxidized products using mass spectrometry. M.C., S.G. and I.H.-G. performed saccharification assays. A.V., C.M. and B.C. carried out microscopy and NMR analyses. L.C. performed the EPR study under the direction of P.H.W. and G.J.D. J.-G.B. supervised the work and organized the data. The manuscript was written by J.-G.B. with contributions from B.H. and P.H.W. All authors made comments on the manuscript and approved the final version. Figures were prepared by J.-G.B., K.E.F., A.L., N.L., S.L., L.C., M.F., S.G. and I.H.-G.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jean-Guy Berrin.

Supplementary information

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    Supplementary Tables 1–4 and Supplementary Figures 1–13

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    Supplementary Data Set 1

    Number of AA14 genes in fungal genomes

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DOI

https://doi.org/10.1038/nchembio.2558