Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity

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...

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Bibliographic Details
Authors: Ruiz Dueñas, Francisco J., Barrasa, José M., Sánchez-García, Marisol, Camarero, Susana, Miyauchi, Shingo, Linde, Dolores, Babiker, Rashid, Drula, Elodie, Ayuso-Fernández, Iván, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, Harald, Castanera Andrés, Raúl, Alfaro Sánchez, Manuel, Ramírez Nasto, Lucía, Pisabarro de Lucas, Gerardo, Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt, Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Vivian, Ng, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David, Martínez, Ángel T.
Format: article
Status:Published version
Publication Date:2021
Country:España
Institution:Universidad Pública de Navarra
Repository:Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
OAI Identifier:oai:academica-e.unavarra.es:2454/41719
Online Access:https://hdl.handle.net/2454/41719
Access Level:Open access
Keyword:Agaricales
Lifestyle evolution
Ignocellulose decay
Plant cell-wall degrading enzymes
Ligninolytic peroxidases
Ancestral-sequence reconstruction
Description
Summary: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 ancestralsequence 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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