Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities

Abstract

Evolution of lignocellulose decomposition was one of the most ecologically important innovations in fungi. White-rot fungi in the Agaricomycetes (mushrooms and relatives) are the most effective microorganisms in degrading both cellulose and lignin components of woody plant cell walls (PCW). However, the precise evolutionary origins of lignocellulose decomposition are poorly understood, largely because certain early-diverging clades of Agaricomycetes and its sister group, the Dacrymycetes, have yet to be sampled, or have been undersampled, in comparative genomic studies. Here, we present new genome sequences of ten saprotrophic fungi, including members of the Dacrymycetes and early-diverging clades of Agaricomycetes (Cantharellales, Sebacinales, Auriculariales, and Trechisporales), which we use to refine the origins and evolutionary history of the enzymatic toolkit of lignocellulose decomposition. We reconstructed the origin of ligninolytic enzymes, focusing on class II peroxidases (AA2), as well as enzymes that attack crystalline cellulose. Despite previous reports of white rot appearing as early as the Dacrymycetes, our results suggest that white-rot fungi evolved later in the Agaricomycetes, with the first class II peroxidases reconstructed in the ancestor of the Auriculariales and residual Agaricomycetes. The exemplars of the most ancient clades of Agaricomycetes that we sampled all lack class II peroxidases, and are thus concluded to use a combination of plesiomorphic and derived PCW degrading enzymes that predate the evolution of white rot.

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.…”

Fungal microbiomes associated with green and non-green building materials

“…dominated the non-green composite bord. The genus Aspergillus includes many infectious fungal species (Richardson and Warnock, 2012) but Peniophora is a genus that causes white rot of wood and includes some plant pathogenic species (Nagy et al, 2016) but is generally not a source of human pathogens.…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…White and brown rot are typical of Basidiomycetes, whereas soft rot is mainly produced by ascomycetes. This broad classification of decay types has been contested recently based partially on comparative genomics of Basidiomycota (74)(75)(76), suggesting that the functional diversity of wood-decay fungi and their role in ecosystems could be better described by a continuum. Several species traditionally classified as white rot fungi lack the enzyme systems to degrade lignin.…”

“…The capacity for white rot presumably evolved in the most recent common ancestor of the Auriculariales and more-derived Agaricomycetes (74,75). Species associated with white rot (e.g., Botryobasidium spp., Tulasnella spp.)…”

“…can be found in earlier-diverging clades too (Cantharellales), but they lack the hallmark enzymes of white rot (76). The symptoms they produce on rotten wood might reflect an ancestral, soft-rot-like wood decomposition strategy (75). White rot has a single evolutionary origin but has been lost several times.…”