Abstract
White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here, we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood-decaying activity within the Basidiomycota genus Pycnoporus. We observed a strong conservation in the genome structures and the repertoires of protein-coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analysed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2-producing enzymes with H2O2-consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 lytic polysaccharide monooxygenase gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood-decaying process.
Highlights
Saprotrophic fungi of Northern Hemisphere and tropical forests impact the carbon cycling through mineralization and alteration of C storage in wood and litter dead organic matter.[1,2] White-rot (WR) fungi are wood decayers with the capacity to mineralize lignin with ultimate formation of CO2 and H2O.3
The genes coding for mating type, Class II peroxidases, CAZymes, peptidases, GSTs, hydrophobins, proteins from the secretory pathway, the glycosylation pathway, the carbon catabolism pathway and small secreted proteins (SSPs) were inspected by expert annotation (Supplementary Tables S2–S15 and Figs S4–S13)
WR fungi are well-studied for the diversity of enzymatic systems for lignocellulose breakdown, their intra-genus diversity has not been extensively explored so far
Summary
Saprotrophic fungi of Northern Hemisphere and tropical forests impact the carbon cycling through mineralization and alteration of C storage in wood and litter dead organic matter.[1,2] White-rot (WR) fungi are wood decayers with the capacity to mineralize lignin with ultimate formation of CO2 and H2O.3. Among WR fungi, the genus Pycnoporus (Basidiomycota, Agaricomycetes) has been studied for the efficiency of lignin degradation, the capacity to secrete laccases and biotechnological applications related to aromatic compound functionalization, biopolymer synthesis and biomass pre-treatment in the pulp and paper industry.[14] Four Pycnoporus species have been differentiated,[15,16] which form a monophyletic group within the Trametes clade.[17] The four species are found in different geo-climatic areas with limited geographical overlap; P. cinnabarinus is widely distributed in the Northern hemisphere, P. coccineus is found in countries bordering the Indian and Pacific Oceans, P. sanguineus is found in the tropics and subtropics of both hemispheres and P. puniceus is found in paleotropical areas.[15,16] The four species are found on stumps and either standing or fallen trunks of deciduous trees
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