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

Ander Peña, Rashid Babiker, Delphine Chaduli, Anna Lipzen, Mei Wang, Mansi Chovatia, Jorge Rencoret, Gisela Marques, Maria Sanchez-Ruiz, Teeratas Kijpornyongpan, Davinia Salvachua, Susana Camarero, Vivian Ng, Ana Gutierrez, Igor Grigoriev, Marie-Noëlle Rosso, Angel Martinez, Francisco Ruiz-Dueñas

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12 Scopus Citations

Abstract

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.

Original languageAmerican English
Article number426
Number of pages31
JournalJournal of Fungi
Volume7
Issue number6
DOIs
StatePublished - 2021

Bibliographical note

Publisher Copyright:
© 2021 by the authors. Licensee MDPI, Basel, Switzerland.

NREL Publication Number

  • NREL/JA-2800-79888

Keywords

  • Carbohydrate-active enzymes
  • Lignin-modifying enzymes
  • Lignocellulose transformation
  • Metabolomics
  • Oxidoreductases
  • Pleurotus eryngii
  • Proteomics
  • Solid-state fermentation
  • Transcriptomics
  • Wheat–straw

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