Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity

Autor: Kurt LaButti, Remedios Pacheco, William Andreopoulos, Mi Yan, Alan Kuo, Anna Lipzen, Raúl Castanera, Francisco J. Ruiz-Dueñas, Iván Ayuso-Fernández, Harald Kellner, Vivian Ng, Guillermo Padilla, Rashid Babiker, Jasmyn Pangilinan, David S. Hibbett, Bernard Henrissat, Patricia Ferreira, Francis Martin, Jorge Barriuso, José María Barrasa, Daniel Cullen, Marisol Sánchez-García, Igor V. Grigoriev, Susana Camarero, Lucía Ramírez, Shingo Miyauchi, Ana Serrano, Manuel Alfaro, Andrew Tritt, Guifen He, Robert Riley, Dolores Linde, Ángel T. Martínez, Marie-Noëlle Rosso, Antonio G. Pisabarro, Elodie Drula
Přispěvatelé: Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa. IMAB - Institute for Multidisciplinary Research in Applied Biology, Ministerio de Economía, Industria y Competitividad (España), National Science Foundation (US), Federal Ministry of Education and Research (Germany), Consejo Superior de Investigaciones Científicas (España), Labex ARBRE, Department of Energy (US), Ruiz-Dueñas, F. J., Barrasa González, José María, Sánchez-García, Marisol, Camarero, Susana, Miyauchi, Shingo, Serrano, Ana, Linde, Dolores, Babiker, Rashid, Drula, Elodie, Ayuso-Fernández, Iván, Padilla, Guillermo, Barriuso, Jorge, Castanera, Raúl, Alfaro, Manuel, Pisabarro, Antonio G., Andreopoulos, William, LaButti, Kurt M., Tritt, Andrew, Lipzen, Anna, He, Guifen, Grigoriev, Igor V., Rosso, Marie-Noëlle, Henrissat, Bernard, Martínez, Ángel T., Ruiz-Dueñas, F. J. [0000-0002-9837-5665], Barrasa González, José María [0000-0002-3904-5375], Sánchez-García, Marisol [0000-0002-0635-6281], Camarero, Susana [0000-0002-2812-895X], Miyauchi, Shingo [0000-0002-0620-5547], Serrano, Ana [0000-0002-7057-0418], Linde, Dolores [0000-0002-0359-0566], Babiker, Rashid [0000-0002-8256-0495], Drula, Elodie [0000-0002-9168-5214], Ayuso-Fernández, Iván [0000-0001-8503-2615], Padilla, Guillermo [0000-0002-5742-4088], Barriuso, Jorge [0000-0003-0916-6560], Castanera, Raúl [0000-0002-3772-7727], Alfaro, Manuel [0000-0002-1130-1904], Pisabarro, Antonio G. [0000-0001-6987-5794], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Tritt, Andrew [0000-0002-1617-449X], Lipzen, Anna [0000-0003-2293-9329], He, Guifen [0000-0003-0433-2822], Grigoriev, Igor V. [0000-0002-3136-8903], Rosso, Marie-Noëlle [0000-0001-8317-7220], Henrissat, Bernard [0000-0002-3434-8588], Martínez, Ángel T. [0000-0002-1584-2863], Centro de Investigaciones Biológicas Margarita Salas, 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), AgroParisTech-Office National des Forêts (ONF)-Université de Lorraine (UL)-Centre National de la Propriété Forestière-CRITT Bois-European Forest Institute = Institut Européen de la Forêt = Euroopan metsäinstituutti (EFI)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Echave, Julian
Jazyk: angličtina
Rok vydání: 2021
Předmět:
[SDV]Life Sciences [q-bio]
Ancestral-sequence reconstruction
Context (language use)
AcademicSubjects/SCI01180
Lignin
Agaricomycetes
03 medical and health sciences
Oxidative enzyme
Genetics
Ignocellulose decay
Agaricales
ancestral-sequence reconstruction
Polyporales
Ligninolytic peroxidases
lifestyle evolution
lignocellulose decay
Molecular Biology
Ecology
Evolution
Behavior and Systematics
Discoveries
ComputingMilieux_MISCELLANEOUS
Ecosystem
Phylogeny
030304 developmental biology
Laccase
0303 health sciences
Evolutionary Biology
Genome
plant cell-wall degrading enzymes
biology
030306 microbiology
AcademicSubjects/SCI01130
Basidiomycota
Lifestyle evolution
15. Life on land
ligninolytic peroxidases
biology.organism_classification
Fungal
Peroxidases
Evolutionary biology
Multigene Family
[SDE]Environmental Sciences
Biochemistry and Cell Biology
Plant cell-wall degrading enzymes
Genome
Fungal
Russulales
Zdroj: Molecular biology and evolution, vol 38, iss 4
Digital.CSIC. Repositorio Institucional del CSIC
instname
Molecular Biology and Evolution
Molecular Biology and Evolution, 2020, 38 (4), p. 1428-1446. ⟨10.1093/molbev/msaa301⟩
Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
Zaguán. Repositorio Digital de la Universidad de Zaragoza
Molecular Biology and Evolution, Oxford University Press (OUP), 2020, 38 (4), pp.1428-1446. ⟨10.1093/molbev/msaa301⟩
ISSN: 0737-4038
1537-1719
Popis: 19 p.-6 fig.
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.
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 für Bildung und Forschung (CEFOX 031B0831B to H.K.); Deutsche Forschungsgemeinschaft (Biodiversity-Exploratories BLD-MFD-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-0002-01), 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.
Databáze: OpenAIRE
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