Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity

  • Francisco J Ruiz-Dueñas
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • José M Barrasa
    Life Sciences Department, Alcalá University, Alcalá de Henares, Spain
  • Marisol Sánchez-García
    Biology Department, Clark University, Worcester, MA, USA
  • Susana Camarero
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Shingo Miyauchi
    INRAE, Laboratory of Excellence ARBRE, Champenoux, France
  • Ana Serrano
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Dolores Linde
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Rashid Babiker
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Elodie Drula
    Architecture et Fonction des Macromolécules Biologiques, CNRS/Aix-Marseille University, Marseille, France
  • Iván Ayuso-Fernández
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Remedios Pacheco
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Guillermo Padilla
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Patricia Ferreira
    Biochemistry and Molecular and Cellular Biology Department and BIFI, Zaragoza University, Zaragoza, Spain
  • Jorge Barriuso
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
  • Harald Kellner
    International Institute Zittau, Technische Universität Dresden, Zittau, Germany
  • Raúl Castanera
    Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
  • Manuel Alfaro
    Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
  • Lucía Ramírez
    Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
  • Antonio G Pisabarro
    Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
  • Robert Riley
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Alan Kuo
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • William Andreopoulos
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Kurt LaButti
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Jasmyn Pangilinan
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Andrew Tritt
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Anna Lipzen
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Guifen He
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Mi Yan
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Vivian Ng
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Igor V Grigoriev
    US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
  • Daniel Cullen
    Forest Products Laboratory, US Department of Agriculture, Madison, WI, USA
  • Francis Martin
    INRAE, Laboratory of Excellence ARBRE, Champenoux, France
  • Marie-Noëlle Rosso
    INRAE, Biodiversité et Biotechnologie Fongiques, Aix-Marseille University, Marseille, France
  • Bernard Henrissat
    Architecture et Fonction des Macromolécules Biologiques, CNRS/Aix-Marseille University, Marseille, France
  • David Hibbett
    Biology Department, Clark University, Worcester, MA, USA
  • Angel T Martínez
    Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain

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<jats:title>Abstract</jats:title> <jats:p>As actors of global carbon cycle, Agaricomycetes (Basidiomycota) have developed complex enzymatic machineries that allow them to decompose all plant polymers, including lignin. Among them, saprotrophic Agaricales are characterized by an unparalleled diversity of habitats and lifestyles. Comparative analysis of 52 Agaricomycetes genomes (14 of them sequenced de novo) reveals that Agaricales possess a large diversity of hydrolytic and oxidative enzymes for lignocellulose decay. Based on the gene families with the predicted highest evolutionary rates—namely cellulose-binding CBM1, glycoside hydrolase GH43, lytic polysaccharide monooxygenase AA9, class-II peroxidases, glucose–methanol–choline oxidase/dehydrogenases, laccases, and unspecific peroxygenases—we reconstructed the lifestyles of the ancestors that led to the extant lignocellulose-decomposing Agaricomycetes. The changes in the enzymatic toolkit of ancestral Agaricales are correlated with the evolution of their ability to grow not only on wood but also on leaf litter and decayed wood, with grass-litter decomposers as the most recent eco-physiological group. In this context, the above families were analyzed in detail in connection with lifestyle diversity. Peroxidases appear as a central component of the enzymatic toolkit of saprotrophic Agaricomycetes, consistent with their essential role in lignin degradation and high evolutionary rates. This includes not only expansions/losses in peroxidase genes common to other basidiomycetes but also the widespread presence in Agaricales (and Russulales) of new peroxidases types not found in wood-rotting Polyporales, and other Agaricomycetes orders. Therefore, we analyzed the peroxidase evolution in Agaricomycetes by ancestral-sequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.</jats:p>

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