Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass

Abstract

BackgroundPlant biomass conversion for green chemistry and bio-energy is a current challenge for a modern sustainable bioeconomy. The complex polyaromatic lignin polymers in raw biomass feedstocks (i.e., agriculture and forestry by-products) are major obstacles for biomass conversions. White-rot fungi are wood decayers able to degrade all polymers from lignocellulosic biomass including cellulose, hemicelluloses, and lignin. The white-rot fungus Polyporus brumalis efficiently breaks down lignin and is regarded as having a high potential for the initial treatment of plant biomass in its conversion to bio-energy. Here, we describe the extraordinary ability of P. brumalis for lignin degradation using its enzymatic arsenal to break down wheat straw, a lignocellulosic substrate that is considered as a biomass feedstock worldwide.ResultsWe performed integrative multi-omics analyses by combining data from the fungal genome, transcriptomes, and secretomes. We found that the fungus possessed an unexpectedly large set of genes coding for Class II peroxidases involved in lignin degradation (19 genes) and GMC oxidoreductases/dehydrogenases involved in generating the hydrogen peroxide required for lignin peroxidase activity and promoting redox cycling of the fungal enzymes involved in oxidative cleavage of lignocellulose polymers (36 genes). The examination of interrelated multi-omics patterns revealed that eleven Class II Peroxidases were secreted by the fungus during fermentation and eight of them where tightly co-regulated with redox cycling enzymatic partners.ConclusionAs a peculiar feature of P. brumalis, we observed gene family extension, up-regulation and secretion of an abundant set of versatile peroxidases and manganese peroxidases, compared with other Polyporales species. The orchestrated secretion of an abundant set of these delignifying enzymes and redox cycling enzymatic partners could contribute to the delignification capabilities of the fungus. Our findings highlight the diversity of wood decay mechanisms present in Polyporales and the potentiality of further exploring this taxonomic order for enzymatic functions of biotechnological interest.Electronic supplementary materialThe online version of this article (10.1186/s13068-018-1198-5) contains supplementary material, which is available to authorized users.

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

“…To untangle the complex responses of poplar and L. bicolor to phytohormones, we performed an unsupervised analysis using the entire gene expression sets derived from RNA‐seq of hormone‐treated colonized and uncolonized poplar LRs, as well as L. bicolor FLM. To this end, we exploited the SHIN+GO pipeline (Miyauchi et al, , , ). On the basis of the normalized levels of the 28,502 transcripts detected in poplar LRs and the 15,129 transcripts detected in L. bicolor mycelia, we built transcriptomic models using the SHIN+GO pipeline on the R platform (Section 2, Data S4 and S5).…”

“…To obtain a comprehensive view of the impact of hormone treatments on the poplar and L. bicolor transcriptomes, we constructed transcriptomic models using SHIN+GO (self‐organizing map harboring informative nodes with gene ontology; Miyauchi et al, , , ). A self‐organizing map was trained with the normalized read count of the selected replicates using Rsomoclu (Wittek et al, ).…”

Mycena genomes resolve the evolution of fungal bioluminescence

“…Mycena species also contain 11–20 copies of AA5_1 (copper radical oxidases), 18–121 copies of AA3_2 (GMC oxidoreductase), and 10–34 copies of AA1_1 (Laccases) 55 . These enzymes are capable of degrading or modifying lignin and are generally in higher abundance in white-rot than in brown-rot fungi 55,56 . For cellulose degradation, white-rot generally has more cellulolytic genes— i.e., GH6 and GH7—and lytic polysaccharide monooxygenase of AA9 than does brown-rot fungi 55 .…”

Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus

“…We integrated SOM with the protein secretome information analysed by peptide-LC-MS/MS, using SOM Harboring Informative Nodes with Gene Ontology. 10 , 47 , 48 …”