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Article

A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material

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Centro de Investigaciones Biológicas Margarita Salas (CIB), Consejo Superior de Investigaciones Científicas (CSIC), 28040 Madrid, Spain
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Institut National de Recherche Pour L’agriculture, L’alimentation et L’environnement (INRAE), Aix Marseille Université, Biodiversité et Biotechnologie Fongiques, 13009 Marseille, France
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Lawrence Berkeley National Laboratory, US Department of Energy (DOE) Joint Genome Institute (JGI), Berkeley, CA 94720, USA
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Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), Consejo Superior de Investigaciones Científicas (CSIC), 41012 Seville, Spain
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Renewable Resources and Enabling Sciences Center, National Renewable Energy Laboratory, Golden, CO 80401, USA
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Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA
*
Author to whom correspondence should be addressed.
Academic Editors: Craig Faulds and Putarak Chomnunti
J. Fungi 2021, 7(6), 426; https://doi.org/10.3390/jof7060426
Received: 30 April 2021 / Revised: 18 May 2021 / Accepted: 26 May 2021 / Published: 28 May 2021
(This article belongs to the Special Issue Exploiting Fungal Solutions for Today's Challenges)
Pleurotus eryngii is a grassland-inhabiting fungus of biotechnological interest due to its ability to colonize non-woody lignocellulosic material. Genomic, transcriptomic, exoproteomic, and metabolomic analyses were combined to explain the enzymatic aspects underlaying wheat–straw transformation. Up-regulated and constitutive glycoside–hydrolases, polysaccharide–lyases, and carbohydrate–esterases active on polysaccharides, laccases active on lignin, and a surprisingly high amount of constitutive/inducible aryl–alcohol oxidases (AAOs) constituted the suite of extracellular enzymes at early fungal growth. Higher enzyme diversity and abundance characterized the longer-term growth, with an array of oxidoreductases involved in depolymerization of both cellulose and lignin, which were often up-regulated since initial growth. These oxidative enzymes included lytic polysaccharide monooxygenases (LPMOs) acting on crystalline polysaccharides, cellobiose dehydrogenase involved in LPMO activation, and ligninolytic peroxidases (mainly manganese-oxidizing peroxidases), together with highly abundant H2O2-producing AAOs. Interestingly, some of the most relevant enzymes acting on polysaccharides were appended to a cellulose-binding module. This is potentially related to the non-woody habitat of P. eryngii (in contrast to the wood habitat of many basidiomycetes). Additionally, insights into the intracellular catabolism of aromatic compounds, which is a neglected area of study in lignin degradation by basidiomycetes, were also provided. The multiomic approach reveals that although non-woody decay does not result in dramatic modifications, as revealed by detailed 2D-NMR and other analyses, it implies activation of the complete set of hydrolytic and oxidative enzymes characterizing lignocellulose-decaying basidiomycetes. View Full-Text
Keywords: Pleurotus eryngii; lignocellulose transformation; solid-state fermentation; wheat–straw; transcriptomics; proteomics; metabolomics; carbohydrate-active enzymes; oxidoreductases; lignin-modifying enzymes Pleurotus eryngii; lignocellulose transformation; solid-state fermentation; wheat–straw; transcriptomics; proteomics; metabolomics; carbohydrate-active enzymes; oxidoreductases; lignin-modifying enzymes
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MDPI and ACS Style

Peña, A.; Babiker, R.; Chaduli, D.; Lipzen, A.; Wang, M.; Chovatia, M.; Rencoret, J.; Marques, G.; Sánchez-Ruiz, M.I.; Kijpornyongpan, T.; Salvachúa, D.; Camarero, S.; Ng, V.; Gutiérrez, A.; Grigoriev, I.V.; Rosso, M.-N.; Martínez, A.T.; Ruiz-Dueñas, F.J. A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material. J. Fungi 2021, 7, 426. https://doi.org/10.3390/jof7060426

AMA Style

Peña A, Babiker R, Chaduli D, Lipzen A, Wang M, Chovatia M, Rencoret J, Marques G, Sánchez-Ruiz MI, Kijpornyongpan T, Salvachúa D, Camarero S, Ng V, Gutiérrez A, Grigoriev IV, Rosso M-N, Martínez AT, Ruiz-Dueñas FJ. A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material. Journal of Fungi. 2021; 7(6):426. https://doi.org/10.3390/jof7060426

Chicago/Turabian Style

Peña, Ander, Rashid Babiker, Delphine Chaduli, Anna Lipzen, Mei Wang, Mansi Chovatia, Jorge Rencoret, Gisela Marques, María I. Sánchez-Ruiz, Teeratas Kijpornyongpan, Davinia Salvachúa, Susana Camarero, Vivian Ng, Ana Gutiérrez, Igor V. Grigoriev, Marie-Noëlle Rosso, Angel T. Martínez, and Francisco J. Ruiz-Dueñas. 2021. "A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material" Journal of Fungi 7, no. 6: 426. https://doi.org/10.3390/jof7060426

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