Comparative genomics of the white-rot fungi, Phanerochaete carnosa and P. chrysosporium, to elucidate the genetic basis of the distinct wood types they colonize

Abstract

BackgroundSoftwood is the predominant form of land plant biomass in the Northern hemisphere, and is among the most recalcitrant biomass resources to bioprocess technologies. The white rot fungus, Phanerochaete carnosa, has been isolated almost exclusively from softwoods, while most other known white-rot species, including Phanerochaete chrysosporium, were mainly isolated from hardwoods. Accordingly, it is anticipated that P. carnosa encodes a distinct set of enzymes and proteins that promote softwood decomposition. To elucidate the genetic basis of softwood bioconversion by a white-rot fungus, the present study reports the P. carnosa genome sequence and its comparative analysis with the previously reported P. chrysosporium genome.ResultsP. carnosa encodes a complete set of lignocellulose-active enzymes. Comparative genomic analysis revealed that P. carnosa is enriched with genes encoding manganese peroxidase, and that the most divergent glycoside hydrolase families were predicted to encode hemicellulases and glycoprotein degrading enzymes. Most remarkably, P. carnosa possesses one of the largest P450 contingents (266 P450s) among the sequenced and annotated wood-rotting basidiomycetes, nearly double that of P. chrysosporium. Along with metabolic pathway modeling, comparative growth studies on model compounds and chemical analyses of decomposed wood components showed greater tolerance of P. carnosa to various substrates including coniferous heartwood.ConclusionsThe P. carnosa genome is enriched with genes that encode P450 monooxygenases that can participate in extractives degradation, and manganese peroxidases involved in lignin degradation. The significant expansion of P450s in P. carnosa, along with differences in carbohydrate- and lignin-degrading enzymes, could be correlated to the utilization of heartwood and sapwood preparations from both coniferous and hardwood species.

Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes

“…Also, peptides corresponding to a GH5 mannanase were identified in cellulose cultures of P. carnosa. In addition, P. carnosa grows better (based on radial growth and mycelium density) on guar gum (galactomannan) than on xylanand pectin-containing substrates (45), thus supporting its preference for softwood bioconversion. Biochemical characterization of P. carnosa hemicellulases is still needed to confirm a correlation between growth profiles and enzyme substrate specificities.…”

“…The chemical compositions of the cell walls of softwoods and hardwoods differ particularly in their hemicelluloses structures (mainly galactoglucomannans are present in softwood, while glucuronoxylan is the most abundant hemicellulose in hardwood) and in the slightly higher lignin contents of softwoods (20). The genome of P. carnosa contains 193 GH gene models, which is higher than the number of gene models in the genome of P. chrysosporium (182 gene models) (45). When the secretome of P. carnosa grown in cellulose and spruce wood cultures was analyzed, the fungus produced a pattern of classical cellulases (GH3 EGs and BGLs and GH6 and -7 CBHs), xylanases (GH10 and -11), debranching hydrolases (GH43), and glucuronoyl esterases (CE1) together with putative LPMOs (AA9) that was similar to the pattern produced by P. chrysosporium (59).…”

“…For example, the wooddecaying white rot fungus Phanerochaete chrysosporium has a larger repertoire of plant cell wall polysaccharide-degrading enzymes than the biotrophic phytopathogen Ustilago maydis, which possesses a minimal set of CAZyme-encoding genes in order to prevent host plant defense responses, as suggested in previous studies (6,8). While it cannot be automatically concluded that an increase in the number of genes related to a particular polysaccharide also means an improved degradation of this polysaccharide, many studies have revealed such correlations (43)(44)(45)(46)(47)(48)(49)(50). However, there are also clear exceptions to this.…”

“…Phanerochaete carnosa, a member of the same genus as P. chrysosporium, is found on softwoods, while most other studied white rot fungi are typically isolated from hardwood (45). The chemical compositions of the cell walls of softwoods and hardwoods differ particularly in their hemicelluloses structures (mainly galactoglucomannans are present in softwood, while glucuronoxylan is the most abundant hemicellulose in hardwood) and in the slightly higher lignin contents of softwoods (20).…”

Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi

“…We have selected (a) 14 popular white rot fungal strains – Ceriporiopsis subvermispora B (Fernandez-Fueyo et al 2012), Heterobasidion annosum v2.0 (Olson et al 2012), Fomitiporia mediterranea v1.0 (Floudas et al 2012), Phanerochaete carnosa HHB-10118 (Suzuki et al 2012), Pycnoporus cinnabarinus BRFM 137 (Levasseur et al 2014), Phanerochaete chrysosporium R78 v2.2 (Martinez et al 2004; Ohm et al 2014), Dichomitus squalens LYAD-421 SS1 (Floudas et al 2012), Trametes versicolor v1.0 (Floudas et al 2012), Punctularia strigosozonata v1.0 (Floudas et al 2012), Phlebia brevispora HHB-7030 SS6 (Binder et al 2013), Botrytis cinerea v1.0 (Amselem et al 2011), Pleurotus ostreatus PC15 v2.0 (Riley et al 2014; Alfaro et al 2016; Castanera et al 2016), Stereum hirsutum FP-91666 SS1 v1.0 (Floudas et al 2012), Pleurotus eryngii ATCC90797 (Guillen et al 1992; Camarero et al 1999; Ruiz‐Dueñas et al 1999; Matheny et al 2006); (b) 15 popular brown rot fungal strains – Postia placenta MAD 698-R v1.0 (Martinez et al 2009), Fibroporia radiculosa TFFH 294 (Tang et al 2012), Wolfiporia cocos MD-104 SS10 v1.0 (Floudas et al 2012), Dacryopinax primogenitus DJM 731 SSP1 v1.0 (Floudas et al 2012), Daedalea quercina v1.0 (Nagy et al 2015), Laetiporus sulphureus var v1.0 (Nagy et al 2015), Postia placenta MAD-698-R-SB12 v1.0 (Martinez et al 2009), Neolentinus lepideus v1.0 (Nagy et al 2015), Serpula lacrymans S7.9 v2.0 (Eastwood et al 2011), Calocera cornea v1.0 (Eastwood et al 2011), Gloeophyllum trabeum v1.0 (Floudas et al 2012), Fistulina hepatica v1.0 (Floudas et al 2015), Fomitopsis pinicola FP-58527 SS1 (Floudas et al 2015), Hydnomerulius pinastri v2.0 (Kohler et al 2015) and Coniophora puteana v1.0 (Kohler et al 2015); (c) 13 popular soft rot fungal strains – Trichoderma reesei v 2.0 (Martinez et al 2008), Rhizopus oryzae 99-880 from Broad (Ma et al 2009), Aspergillus wentii v1.0 (De Vries et al 2017), Penicillium chrysogenum Wisconsin 54-1255 (Van Den Berg et al 2008), Daldinia eschscholzii EC12 v1.0, Hypoxylon sp. CI-4A v1.0 (Wu et al 2017), Aspergillus niger ATCC 1015 v4.0 (Andersen et al 2011), Hypoxylon sp.…”