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 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.

This work was supported by the Spanish Ministry of Economy, Industry and Competitiveness (BIO2017-86559-R to F.J.R.-D., S.C., and A.T.M., BIO2015-7369-JIN to J.B., and AGL2014-55971-R to A.G.P. and L.R., projects cofinanced by FEDER funds); National Science Foundation (grant 1457721 to D.C.); Bundesministerium fur Bildung und Forschung (CEFOX 031B0831B to H.K.); Deutsche Forschungsgemeinschaft (Biodiversity-Exploratories BLDMFD-HZG III, KE 1742/2-1 to H.K.); Consejo Superior de Investigaciones Científicas (PIE-201620E081 to A.T.M.); and the Laboratory of Excellence ARBRE (ANR-11-LABX-000201), the Region Lorraine, the European Regional Development Fund, and the Plant-Microbe Interfaces Scientific Focus Area in the Genomic Science Program, U.S. DOE Office of Science (to F.M.). The work conducted by the JGI, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. DOE under contract DE-AC02-05CH11231.