Genomic analysis enlightens agaricales Lifestyle Evolution and increasing peroxidase diversity
2020
Ruiz-Dueñas, Francisco | Barrasa, José | Sánchez-García, Marisol | Camarero, Susana | Miyauchi, Shingo | Serrano, Ana | Linde, Dolores | Babiker, Rashid | Drula, Elodie | Ayuso-Fernández, Iván | Pacheco, Remedios | Padilla, Guillermo | Ferreira, Patricia | Barriuso, Jorge | Kellner, Harald | Castanera, Raúl | Alfaro, Manuel | Ramirez, Lucía | Pisabarro, Antonio | Riley, Robert | Kuo, Alan | Andreopoulos, William | Labutti, Kurt | Pangilinan, Jasmyn | Tritt, Andrew | Lipzen, Anna | He, Guifen | Yan, Mi | Ng, Vivian | Grigoriev, Igor | Cullen, Daniel | Rosso, Marie-Noëlle | Henrissat, Bernard | Hibbett, David | Martínez, Angel | Centro de Investigaciones Biológicas Margarita Salas (CIB) ; Consejo Superior de Investigaciones Cientificas [España] = Spanish National Research Council [Spain] (CSIC) | LabEx ARBRE : Advanced Research on the Biology of Tree and Forest Ecosystems ([LabEx ARBRE]) ; AgroParisTech-CRITT Bois-Office national des forêts (ONF)-Université de Lorraine (UL)-Centre National de la Propriété Forestière-European Forest Institute = Institut Européen de la Forêt = Euroopan metsäinstituutti (EFI)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Architecture et fonction des macromolécules biologiques (AFMB) ; Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Biodiversité et Biotechnologie Fongiques (BBF) ; Aix Marseille Université (AMU)-École Centrale de Marseille (ECM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Spanish Ministry of Economy, Industry and Competitiveness BIO2017-86559-RBIO2015-7369-JIN AGL2014-55971-RNational Science Foundation (NSF)1457721 Federal Ministry of Education & Research (BMBF) CEFOX 031B0831B Deutsche Forschungsgemeinschaft (Biodiversity-Exploratories BLDMFD-HZG III) KE 1742/2-1Consejo Superior de Investigaciones Cientificas PIE-201620E081United States Department of Energy (DOE) DE-AC02-05CH11231 | ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011)
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Show more [+] Less [-]English. 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 ancestralAgaricales 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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