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1. El análisis de 52 genomas fúngicos aclara la evolución de los estilos de vida de los Agaricales

Author

Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), National Science Foundation (US), Consejo Superior de Investigaciones Científicas (España), Agence Nationale de la Recherche (France), University of California, Berkeley, Ruiz-Dueñas, F. J. [0000-0002-9837-5665], 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], Ramírez, Lucía [0000-0002-0023-4240], Pisabarro, Antonio G. [0000-0001-6987-5794], Riley, Robert [0000-0003-0224-0975], Kuo, Alan [0000-0003-3514-3530], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Pangilinan, Jasmyn [0000-0001-7966-3496], 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], Hibbett, David S. [0000-0002-9145-3165], Martínez, Ángel T. [0000-0002-1584-2863], 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, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, H., Castanera, Raúl, Alfaro, Manuel, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Ng, Vivian, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., Martínez, Ángel T., Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), National Science Foundation (US), Consejo Superior de Investigaciones Científicas (España), Agence Nationale de la Recherche (France), University of California, Berkeley, Ruiz-Dueñas, F. J. [0000-0002-9837-5665], 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], Ramírez, Lucía [0000-0002-0023-4240], Pisabarro, Antonio G. [0000-0001-6987-5794], Riley, Robert [0000-0003-0224-0975], Kuo, Alan [0000-0003-3514-3530], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Pangilinan, Jasmyn [0000-0001-7966-3496], 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], Hibbett, David S. [0000-0002-9145-3165], Martínez, Ángel T. [0000-0002-1584-2863], 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, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, H., Castanera, Raúl, Alfaro, Manuel, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Ng, Vivian, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., and Martínez, Ángel T.

Abstract

Los Agaricomycetes han desarrollado complejas maquinarias enzimáticas que les permiten descomponer los diferentes polímeros vegetales, incluida la lignina. Entre ellos, los Agaricales saprótrofos se caracterizan por su diversidad de hábitats y estilos de vida. El análisis de 52 genomas de Agaricomycetes aquí realizado revela que los Agaricales poseen una gran diversidad de enzimas hidrolíticas y oxidativas para la descomposición de la lignocelulosa. En base a las familias de genes con mayor velocidad evolutiva (dominios de unión a celulosa, glicosil hidrolasa GH43, monooxigenasas líticas de polisacáridos, peroxidasas ligninolíticas, enzimas de la superfamilia de glucosa-metanol-colina oxidasas/deshidrogenasas, lacasas y peroxigenasas), reconstruimos los estilos de vida de los ancestros que dieron lugar a los actuales Agaricomycetes degradadores de lignocelulosa. Los cambios en el conjunto de herramientas enzimáticas de los Agaricales ancestrales se correlacionaron con la evolución de su capacidad para crecer no solo sobre madera, sino también sobre hojarasca de bosques y madera en descomposición, siendo los descomponedores de la hojarasca de praderas el grupo ecofisiológico más reciente. En este contexto, las anteriores familias de enzimas se analizaron en relación con la diversidad de estilos de vida. Las peroxidasas aparecen como un componente central del set enzimático de los Agaricomycetes saprotrófos, consistente con su papel esencial en la degradación de la lignina y sus altas tasas evolutivas. Esto incluye no solo expansiones/pérdidas de genes de peroxidasas, sino también la presencia generalizada en Agaricales de nuevos tipos de peroxidasas que no se encuentran en Polyporales degradadores de madera, y en otros órdenes de Agaricomycetes.

Published
2021

2. Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay

Author

Joint Genome Institute (US), Institut Carnot Pasteur MS, l’Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (France), Conseil Régional Provence-Alpes-Côte d'Azur, Centre National de la Recherche Scientifique (France), Labex ARBRE, Conseil Régional de Lorraine, European Commission, Hungarian Academy of Sciences, Ministerio de Economía, Industria y Competitividad (España), Consejo Superior de Investigaciones Científicas (España), Agencia Estatal de Investigación (España), Ministerio de Ciencia, Innovación y Universidades (España), Czech Science Foundation, Hage, Hayat [0000-0003-4118-1816], Miyauchi, Shingo [0000-0002-0620-5547], Virágh, Máté [0000-0002-2278-1288], Drula, Elodie [0000-0002-9168-5214], Min, Byoungnam [0000-0002-7469-088X], Favel, Anne [0000-0003-2255-3637], Lesage-Meessen, Laurence [0000-0003-2275-2978], Merényi, Z. [0000-0003-1114-3739], Eugenio, Laura I. de [0000-0002-0496-8663], Morin, Emmanuelle [0000-0002-7268-972X], Martínez, Ángel T. [0000-0002-1584-2863], Baldrian, Petr [0000-0002-8983-2721], Stursová, Martina [0000-0003-1387-6426], Martínez, María Jesús [0000-0003-2166-1097], Novotny, Cenek [0000-0003-3274-471X], Maurice, Sundy [0000-0002-5376-0981], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Na, Hyunsoo [0000-0002-4386-017X], Barry, Kerrie [0000-0002-8999-6785], Lipzen, Anna [0000-0003-2293-9329], Henrissat, Bernard [0000-0002-3434-8588], Ahrendt, Steven [0000-0002-3029-2126], Grigoriev, Igor V. [0000-0002-3136-8903], Rosso, Marie-Noëlle [0000-0001-8317-7220], Hage, Hayat, Miyauchi, Shingo, Virágh, Máté, Drula, Elodie, Min, Byoungnam, Chaduli, Delphine, Navarro, David, Favel, Anne, Norest, Manon, Lesage-Meessen, Laurence, Bálint, Balázs, Merényi, Z., Eugenio, Laura I. de, Morin, Emmanuelle, Martínez, Ángel T., Baldrian, Petr, Stursová, Martina, Martínez, María Jesús, Novotny, Cenek, Magnuson, Jon K., Spatafora, Joey W., Maurice, Sundy, Pangilinan, Jasmyn, Andreopoulos, William, LaButti, Kurt M., Hundley, Hope, Na, Hyunsoo, Kuo, Alan, Barry, Kerrie, Lipzen, Anna, Henrissat, Bernard, Riley, Robert, Ahrendt, Steven, Nagy, Lazslo G., Grigoriev, Igor V., Martin, Francis, Rosso, Marie-Noëlle, Joint Genome Institute (US), Institut Carnot Pasteur MS, l’Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (France), Conseil Régional Provence-Alpes-Côte d'Azur, Centre National de la Recherche Scientifique (France), Labex ARBRE, Conseil Régional de Lorraine, European Commission, Hungarian Academy of Sciences, Ministerio de Economía, Industria y Competitividad (España), Consejo Superior de Investigaciones Científicas (España), Agencia Estatal de Investigación (España), Ministerio de Ciencia, Innovación y Universidades (España), Czech Science Foundation, Hage, Hayat [0000-0003-4118-1816], Miyauchi, Shingo [0000-0002-0620-5547], Virágh, Máté [0000-0002-2278-1288], Drula, Elodie [0000-0002-9168-5214], Min, Byoungnam [0000-0002-7469-088X], Favel, Anne [0000-0003-2255-3637], Lesage-Meessen, Laurence [0000-0003-2275-2978], Merényi, Z. [0000-0003-1114-3739], Eugenio, Laura I. de [0000-0002-0496-8663], Morin, Emmanuelle [0000-0002-7268-972X], Martínez, Ángel T. [0000-0002-1584-2863], Baldrian, Petr [0000-0002-8983-2721], Stursová, Martina [0000-0003-1387-6426], Martínez, María Jesús [0000-0003-2166-1097], Novotny, Cenek [0000-0003-3274-471X], Maurice, Sundy [0000-0002-5376-0981], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Na, Hyunsoo [0000-0002-4386-017X], Barry, Kerrie [0000-0002-8999-6785], Lipzen, Anna [0000-0003-2293-9329], Henrissat, Bernard [0000-0002-3434-8588], Ahrendt, Steven [0000-0002-3029-2126], Grigoriev, Igor V. [0000-0002-3136-8903], Rosso, Marie-Noëlle [0000-0001-8317-7220], Hage, Hayat, Miyauchi, Shingo, Virágh, Máté, Drula, Elodie, Min, Byoungnam, Chaduli, Delphine, Navarro, David, Favel, Anne, Norest, Manon, Lesage-Meessen, Laurence, Bálint, Balázs, Merényi, Z., Eugenio, Laura I. de, Morin, Emmanuelle, Martínez, Ángel T., Baldrian, Petr, Stursová, Martina, Martínez, María Jesús, Novotny, Cenek, Magnuson, Jon K., Spatafora, Joey W., Maurice, Sundy, Pangilinan, Jasmyn, Andreopoulos, William, LaButti, Kurt M., Hundley, Hope, Na, Hyunsoo, Kuo, Alan, Barry, Kerrie, Lipzen, Anna, Henrissat, Bernard, Riley, Robert, Ahrendt, Steven, Nagy, Lazslo G., Grigoriev, Igor V., Martin, Francis, and Rosso, Marie-Noëlle

Abstract

Because they comprise some of the most efficient wood-decayers, Polyporales fungi impact carbon cycling in forest environment. Despite continuous discoveries on the enzymatic machinery involved in wood decomposition, the vision on their evolutionary adaptation to wood decay and genome diversity remains incomplete., We combined the genome sequence information from 50 Polyporales species, including 26 newly sequenced genomes and sought for genomic and functional adaptations to wood decay through the analysis of genome composition and transcriptome responses to different carbon sources.The genomes of Polyporales from different phylogenetic clades showed poor conservation in macrosynteny, indicative of genome rearrangements. We observed different gene family expansion/contraction histories for plant cell wall degrading enzymes in core polyporoids and phlebioids and captured expansions for genes involved in signaling and regulation in the lineages of white rotters. Furthermore, we identified conserved cupredoxins, thaumatin-like proteins and Lytic Polysaccharide Monooxygenases with a yet uncharacterized appended module as new candidate players in wood decomposition.Given the current need for enzymatic toolkits dedicated to the transformation of renewable carbon sources, the observed genomic diversity among Polyporales strengthens the relevance of mining Polyporales biodiversity to understand the molecular mechanisms of wood decay.

Published
2021

3. Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity

Author

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. [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], 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, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, H., Castanera, Raúl, Alfaro, Manuel, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Ng, Vivian, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., Martínez, Ángel T., 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. [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], 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, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, H., Castanera, Raúl, Alfaro, Manuel, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Ng, Vivian, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., and Martínez, Ángel T.

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

Published
2020

4. El análisis de 52 genomas fúngicos aclara la evolución de los estilos de vida de los Agaricales

Author

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, Pacheco, Remedios, Padilla, Guillermo, Ferreira, Patricia, Barriuso, Jorge, Kellner, H., Castanera, Raúl, Alfaro, Manuel, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Yan, Mi, Ng, Vivian, Grigoriev, Igor V., Cullen, Daniel, Martin, Francis, Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., Martínez, Ángel T., Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), National Science Foundation (US), Consejo Superior de Investigaciones Científicas (España), Agence Nationale de la Recherche (France), University of California, Berkeley, Ruiz-Dueñas, F. J., 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, Ramírez, Lucía, Pisabarro, Antonio G., Riley, Robert, Kuo, Alan, Andreopoulos, William, LaButti, Kurt M., Pangilinan, Jasmyn, Tritt, Andrew, Lipzen, Anna, He, Guifen, Grigoriev, Igor V., Rosso, Marie-Noëlle, Henrissat, Bernard, Hibbett, David S., Martínez, Ángel T., Ruiz-Dueñas, F. J. [0000-0002-9837-5665], 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], Ramírez, Lucía [0000-0002-0023-4240], Pisabarro, Antonio G. [0000-0001-6987-5794], Riley, Robert [0000-0003-0224-0975], Kuo, Alan [0000-0003-3514-3530], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Pangilinan, Jasmyn [0000-0001-7966-3496], 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], Hibbett, David S. [0000-0002-9145-3165], and Martínez, Ángel T. [0000-0002-1584-2863]

Abstract

1 p., Los Agaricomycetes han desarrollado complejas maquinarias enzimáticas que les permiten descomponer los diferentes polímeros vegetales, incluida la lignina. Entre ellos, los Agaricales saprótrofos se caracterizan por su diversidad de hábitats y estilos de vida. El análisis de 52 genomas de Agaricomycetes aquí realizado revela que los Agaricales poseen una gran diversidad de enzimas hidrolíticas y oxidativas para la descomposición de la lignocelulosa. En base a las familias de genes con mayor velocidad evolutiva (dominios de unión a celulosa, glicosil hidrolasa GH43, monooxigenasas líticas de polisacáridos, peroxidasas ligninolíticas, enzimas de la superfamilia de glucosa-metanol-colina oxidasas/deshidrogenasas, lacasas y peroxigenasas), reconstruimos los estilos de vida de los ancestros que dieron lugar a los actuales Agaricomycetes degradadores de lignocelulosa. Los cambios en el conjunto de herramientas enzimáticas de los Agaricales ancestrales se correlacionaron con la evolución de su capacidad para crecer no solo sobre madera, sino también sobre hojarasca de bosques y madera en descomposición, siendo los descomponedores de la hojarasca de praderas el grupo ecofisiológico más reciente. En este contexto, las anteriores familias de enzimas se analizaron en relación con la diversidad de estilos de vida. Las peroxidasas aparecen como un componente central del set enzimático de los Agaricomycetes saprotrófos, consistente con su papel esencial en la degradación de la lignina y sus altas tasas evolutivas. Esto incluye no solo expansiones/pérdidas de genes de peroxidasas, sino también la presencia generalizada en Agaricales de nuevos tipos de peroxidasas que no se encuentran en Polyporales degradadores de madera, y en otros órdenes de Agaricomycetes., Projectos/contratos BIO2017-86559-R, BIO2015-73697-JIN, AGL2014-55971-R, NSF-grant-1457721, CEFOX-031B0831B, PIE-201620E081, ANR-11-LABX-0002-01, US-DOE-DE-AC02-05CH11231

Published
2021

5. Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay

Author

Hayat, Hage, Shingo, Miyauchi, Máté, Virágh, Elodie, Drula, Byoungnam, Min, Delphine, Chaduli, David, Navarro, Anne, Favel, Manon, Norest, Laurence, Lesage-Meessen, Balázs, Bálint, Zsolt, Merényi, Laura, de Eugenio, Emmanuelle, Morin, Angel T, Martínez, Petr, Baldrian, Martina, Štursová, María Jesús, Martínez, Cenek, Novotny, Jon K, Magnuson, Joey W, Spatafora, Sundy, Maurice, Jasmyn, Pangilinan, Willian, Andreopoulos, Kurt, LaButti, Hope, Hundley, Hyunsoo, Na, Alan, Kuo, Kerrie, Barry, Anna, Lipzen, Bernard, Henrissat, Robert, Riley, Steven, Ahrendt, László G, Nagy, Igor V, Grigoriev, Francis, Martin, Marie-Noëlle, Rosso, 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), Max Planck Institute for Plant Breeding Research (MPIPZ), Biological Research Centre [Szeged] (BRC), 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), US Department of Energy Joint Genome Institute, University of California, Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Centro de Investigaciones Biológicas Margarita Salas, Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institute of Microbiology of the ASCR, v. v. i. [Prague, Czech Republic], Technical University of Ostrava [Ostrava] (VSB), Pacific Northwest National Laboratory (PNNL), Department of Botany and Plant Pathology, Oregon State University (OSU), University of Oslo (UiO), King Abdulaziz University, Institute of Biology [Budapest], Faculty of Sciences [Budapest], Eötvös Loránd University (ELTE)-Eötvös Loránd University (ELTE), United States Department of Energy (DOE) DE-AC02-05CH11231DE-SC0019427Institut Carnot 3BCARRegion Provence-Alpes-Cote d'AzurGroupement de Recherche Genomique EnvironnementaleRegion Grand-EstEuropean CommissionHungarian Academy of Sciences' Momentum Program LP2019-13/2019Spanish Ministry of Economy, Industry and Competitiveness BIO2017-86559-RConsejo Superior de Investigaciones Cientificas PIE-201620E081Agencia Estatal de InvestigacionMinistry of Science, Innovation and Universities RTI2018-093683-B-I00Grant Agency of the Czech Republic 17-20110SFrench National Research Institute for Agriculture, Food and Environment, ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011), University of California (UC), Joint Genome Institute (US), Institut Carnot Pasteur MS, l’Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (France), Conseil Régional Provence-Alpes-Côte d'Azur, Centre National de la Recherche Scientifique (France), Labex ARBRE, Conseil Régional de Lorraine, European Commission, Hungarian Academy of Sciences, Ministerio de Economía, Industria y Competitividad (España), Consejo Superior de Investigaciones Científicas (España), Agencia Estatal de Investigación (España), Ministerio de Ciencia, Innovación y Universidades (España), Czech Science Foundation, Hage, Hayat, Miyauchi, Shingo, Virágh, Máté, Drula, Elodie, Min, Byoungnam, Favel, Anne, Lesage-Meessen, Laurence, Merényi, Z., Eugenio, Laura I. de, Morin, Emmanuelle, Martínez, Ángel T., Baldrian, Petr, Stursová, Martina, Martínez, María Jesús, Novotny, Cenek, Maurice, Sundy, Andreopoulos, William, LaButti, Kurt M., Na, Hyunsoo, Barry, Kerrie, Lipzen, Anna, Henrissat, Bernard, Ahrendt, Steven, Grigoriev, Igor V., Rosso, Marie-Noëlle, Hage, Hayat [0000-0003-4118-1816], Miyauchi, Shingo [0000-0002-0620-5547], Virágh, Máté [0000-0002-2278-1288], Drula, Elodie [0000-0002-9168-5214], Min, Byoungnam [0000-0002-7469-088X], Favel, Anne [0000-0003-2255-3637], Lesage-Meessen, Laurence [0000-0003-2275-2978], Merényi, Z. [0000-0003-1114-3739], Eugenio, Laura I. de [0000-0002-0496-8663], Morin, Emmanuelle [0000-0002-7268-972X], Martínez, Ángel T. [0000-0002-1584-2863], Baldrian, Petr [0000-0002-8983-2721], Stursová, Martina [0000-0003-1387-6426], Martínez, María Jesús [0000-0003-2166-1097], Novotny, Cenek [0000-0003-3274-471X], Maurice, Sundy [0000-0002-5376-0981], Andreopoulos, William [0000-0001-9097-1123], LaButti, Kurt M. [0000-0002-5838-1972], Na, Hyunsoo [0000-0002-4386-017X], Barry, Kerrie [0000-0002-8999-6785], Lipzen, Anna [0000-0003-2293-9329], Henrissat, Bernard [0000-0002-3434-8588], Ahrendt, Steven [0000-0002-3029-2126], Grigoriev, Igor V. [0000-0002-3136-8903], and Rosso, Marie-Noëlle [0000-0001-8317-7220]

Subjects
Special Issue Articles, [SDV]Life Sciences [q-bio], Wood decay, Microbiology, Fungal Proteins, Genetics, Plant cell wall, Fungal ecology, Phylogeny, Evolutionary Biology, Genome, Basidiomycota, Human Genome, Special Issue Article, Phylogenomics, Biodiversity, Wood, Climate Action, Fungal, Genome, Fungal, Polyporales, Transcriptome, Lignocellulose, CAZymes, Biotechnology
Abstract

17 p.-7 fig., Because they comprise some of the most efficient wood-decayers, Polyporales fungi impact carbon cycling in forest environment. Despite continuous discoveries on the enzymatic machinery involved in wood decomposition, the vision on their evolutionary adaptation to wood decay and genome diversity remains incomplete., We combined the genome sequence information from 50 Polyporales species, including 26 newly sequenced genomes and sought for genomic and functional adaptations to wood decay through the analysis of genome composition and transcriptome responses to different carbon sources.The genomes of Polyporales from different phylogenetic clades showed poor conservation in macrosynteny, indicative of genome rearrangements. We observed different gene family expansion/contraction histories for plant cell wall degrading enzymes in core polyporoids and phlebioids and captured expansions for genes involved in signaling and regulation in the lineages of white rotters. Furthermore, we identified conserved cupredoxins, thaumatin-like proteins and Lytic Polysaccharide Monooxygenases with a yet uncharacterized appended module as new candidate players in wood decomposition.Given the current need for enzymatic toolkits dedicated to the transformation of renewable carbon sources, the observed genomic diversity among Polyporales strengthens the relevance of mining Polyporales biodiversity to understand the molecular mechanisms of wood decay., This work was supported by the U.S. Department of Energy Joint Genome Institute, a Department of Energy Office of Science User Facility (grant # DE-AC02-05CH11231, DESC0019427 to I.V.G. and B.M.); Institut Carnot 3BCAR, the French National Research Institute for Agriculture, Food and Environment, The Region Provence Alpes Côte d’Azur and the Groupement de Recherche Génomique Environnementale to H.H.; the Laboratory of Excellence ARBRE (grant # ANR-11-LABX-0002-01 to F.M.); the Region Lorraine and the European Regional Development Fund to F.M.; the Hungarian Academy of Sciences’ Momentum Program (grant # LP2019-13/2019 to L.G.N.); the Spanish Ministry of Economy, Industry and Competitiveness (grant # BIO2017-86559-R to A.T.M.); the Consejo Superior de Investigaciones Científicas (grant # PIE-201620E081 to A.T.M.); the Agencia Estatal de Investigación, the European Regional Development Fund and the Ministry of Science, Innovation and Universities (grant # RTI2018-093683-B-I00 to L.D.E. and M.J.M.) and the Czech Science Foundation (grant# 17-20110S to P.B. and M.Š.).

Published
2021
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6. Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity

Author

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, 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), and Echave, Julian

Subjects
[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
Abstract

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.

Published
2021
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