Publication:
Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity

Date

2021

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

Director

Publisher

Oxford University Press
Acceso abierto / Sarbide irekia
Artículo / Artikulua
Versión publicada / Argitaratu den bertsioa

Project identifier

AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-86559-R/ES/recolecta
MINECO//BIO2015-73697-JIN/ES/recolecta
MINECO//AGL2014-55971-R/ES/recolecta
Métricas Alternativas

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 ancestralsequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.

Description

Keywords

Agaricales, Lifestyle evolution, Ignocellulose decay, Plant cell-wall degrading enzymes, Ligninolytic peroxidases, Ancestral-sequence reconstruction

Department

Institute for Multidisciplinary Research in Applied Biology - IMAB

Faculty/School

Degree

Doctorate program

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