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

Abstract

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. We performed integrative multi-omics analyses by combining data from the fungal genome, transcriptomes, and secretomes. We found the fungus possessed an unexpectedly large set of genes coding for enzymes related to lignin degradation, and that these were highly expressed and massively secreted under solid-state fermentation conditions. The examination of interrelated multi-omics patterns revealed the coordinated regulation of lignin-active peroxidases and H2O2-generating enzymes along with the activation of cellular mechanisms for detoxification, which combined to result in the efficient lignin breakdown by the fungus.

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

“…These findings support a role for these proteins in wood decay and are congruent with the previously observed upregulation of these genes and the secretion of peptidases during growth on lignocellulosic substrates (e.g. this study; Hori et al, 2014;Korripally et al, 2015;Miyauchi et al, 2017Miyauchi et al, , 2018Moudy and Stites, 2017). In early Polyporales, we also observed gene expansion for several groups of regulator families, including F-box domain proteins, transcription factors, BTB/POZ proteins, RING/MYND type zinc finger proteins, LLR domain proteins and protein kinases.…”

Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

“…5d) are also predicted for Arg-AA9 protein sequences (presented here in Fig. 2 and Table 1 and previously (34,35,38)), for which the transcription of the corresponding genes were upregulated during fungal growth on plant biomass. In addition, in the Fungi Phosphorylation Database (FPD) (50) documented Ser phosphorylation sites in fungal species (including Aspergillus) can be found which are consistent with the LsAA9B sequence surrounding the S25 phosphorylation, supporting the notion that phosphorylation could play a role in fungal plant biomass degradation.…”

“…To augment previous reports on transcriptional regulation of Arg-AA9-encoding genes during fungal growth on plant biomass (33)(34)(35), we sought additional evidence in other fungal species. Using RNAseq analysis (as previously described in (38)), we identified a number of genes in several Polyporales species (with around 70% sequence identity to LsAA9B, Fig.…”

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

“…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, 2016Miyauchi et al, , 2017Miyauchi et al, , 2018. A self-organizing map was trained with the normalized read count of the selected replicates using Rsomoclu (Wittek et al, 2017).…”

“…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, 2016(Miyauchi et al, , 2017(Miyauchi et al, , 2018. 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).…”