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Journal Articles Molecular Biology and Evolution Year : 2020

Genomic analysis enlightens agaricales Lifestyle Evolution and increasing peroxidase diversity

José Barrasa
  • Function : Author
Marisol Sánchez-García
  • Function : Author
Susana Camarero
Ana Serrano
  • Function : Author
Dolores Linde
Rashid Babiker
  • Function : Author
Iván Ayuso-Fernández
  • Function : Author
Remedios Pacheco
  • Function : Author
Guillermo Padilla
  • Function : Author
Patricia Ferreira
  • Function : Author
Jorge Barriuso
  • Function : Author
Harald Kellner
  • Function : Author
Raúl Castanera
  • Function : Author
Manuel Alfaro
  • Function : Author
Lucía Ramirez
  • Function : Author
Antonio Pisabarro
  • Function : Author
Robert Riley
  • Function : Author
Alan Kuo
William Andreopoulos
  • Function : Author
Kurt Labutti
Jasmyn Pangilinan
  • Function : Author
Andrew Tritt
  • Function : Author
Anna Lipzen
Guifen He
  • Function : Author
Mi Yan
  • Function : Author
Vivian Ng
Igor Grigoriev
Daniel Cullen
  • Function : Author
David Hibbett
  • Function : Author
Angel Martínez
  • Function : Author

Abstract

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
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hal-03099933 , version 1 (25-04-2022)

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Francisco Ruiz-Dueñas, José Barrasa, Marisol Sánchez-García, Susana Camarero, Shingo Miyauchi, et al.. Genomic analysis enlightens agaricales Lifestyle Evolution and increasing peroxidase diversity. Molecular Biology and Evolution, 2020, 38 (4), p. 1428-1446. ⟨10.1093/molbev/msaa301⟩. ⟨hal-03099933⟩
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