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.
Highlights
Lignocellulose is the most abundant component of Earth’s biomass, with over 180 billion tons produced annually [1]
497 proteins (3% of the overall encoded proteins) constitute the repertoire of: (i) glycoside hydrolase (GH, 239 enzymes), polysaccharide lyase (PL, 33 enzymes) and carbohydrate esterase (CE, 26 enzymes) CAZymes; (ii) carbohydratebinding modules (CBMs, 95 modules); and (iii) oxidoreductases classified as Auxiliary
(Figure 2) would be the result of the early adaptation of P. eryngii to the lignocellulosic substrate, while the small changes that occurred in long-term wheat–straw culture were interpreted as a nearly complete metabolic adaptation to grow on this substrate
Summary
Lignocellulose is the most abundant component of Earth’s biomass, with over 180 billion tons produced annually [1]. Many basidiomycete fungi can grow on lignocellulosic materials Their ability and efficiency to degrade lignocellulose largely depend on the repertoire of hydrolytic and oxidative enzymes able to act on the plant cell-wall polymers [6,7,8]. White-rot basidiomycetes are the only ones capable of efficiently degrading lignin, the aromatic polymer that protects cell-wall polysaccharides from microbial and enzymatic attack Due to this unique capability, white-rot fungi play a key role in carbon recycling in land ecosystems and provide valuable biotechnological tools for processing plant biomass in lignocellulose biorefineries [9,10]
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