Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion

Abstract

Brown-rot fungi such as Postia placenta are common inhabitants of forest ecosystems and are also largely responsible for the destructive decay of wooden structures. Rapid depolymerization of cellulose is a distinguishing feature of brown-rot, but the biochemical mechanisms and underlying genetics are poorly understood. Systematic examination of the P. placenta genome, transcriptome, and secretome revealed unique extracellular enzyme systems, including an unusual repertoire of extracellular glycoside hydrolases. Genes encoding exocellobiohydrolases and cellulose-binding domains, typical of cellulolytic microbes, are absent in this efficient cellulose-degrading fungus. When P. placenta was grown in medium containing cellulose as sole carbon source, transcripts corresponding to many hemicellulases and to a single putative ␤-1-4 endoglucanase were expressed at high levels relative to glucose-grown cultures. These transcript profiles were confirmed by direct identification of peptides by liquid chromatography-tandem mass spectrometry (LC-MS/MS). Also upregulated during growth on cellulose medium were putative iron reductases, quinone reductase, and structurally divergent oxidases potentially involved in extracellular generation of Fe(II) and H2O2. These observations are consistent with a biodegradative role for Fenton chemistry in which Fe(II) and H2O2 react to form hydroxyl radicals, highly reactive oxidants capable of depolymerizing cellulose. The P. placenta genome resources provide unparalleled opportunities for investigating such unusual mechanisms of cellulose conversion. More broadly, the genome offers insight into the diversification of lignocellulose degrading mechanisms in fungi. Comparisons with the closely related white-rot fungus Phanerochaete chrysosporium support an evolutionary shift from white-rot to brown-rot during which the capacity for efficient depolymerization of lignin was lost.cellulose ͉ fenton ͉ lignin ͉ cellulase ͉ brown-rot

Mode of action of brown rot decay resistance in modified wood: a review

“…Brown rot wood degradation has been studied mainly based on Gloeophyllum trabeum, although some mechanisms have also been confirmed in Postia placenta, Serpula lacrymans, and others (Goodell et al 1997;Shimokawa et al 2004;Martinez et al 2009). Differences between species have also been reported, which support the theory of the repeated evolution of brown rot fungi from white rot fungi (Green and Highley 1996;Hibbett and Donoghue 2001;Niemenmaa et al 2008;Kang et al 2009).…”

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.…”

Investigating Aspergillus nidulans secretome during colonisation of cork cell walls

“…Phanerochaete chrysosporium) or in Fenton-type reactions (brown rot fungi, e.g. Pleurotus eryngii and Postia placenta) [65,66]. The genome of A. nidulans contains genes putatively encoding for peroxidases [42,67].…”