The genome sequence of the commercially cultivated mushroom Agrocybe aegerita reveals a conserved repertoire of fruiting-related genes and a versatile suite of biopolymer-degrading enzymes

Abstract

Background: Agrocybe aegerita is an agaricomycete fungus with typical mushroom features, which is commercially cultivated for its culinary use. In nature, it is a saprotrophic or facultative pathogenic fungus causing a white-rot of hardwood in forests of warm and mild climate. The ease of cultivation and fructification on solidified media as well as its archetypal mushroom fruit body morphology render A. aegerita a well-suited model for investigating mushroom developmental biology.

Results: Here, the genome of the species is reported and analysed with respect to carbohydrate active genes and genes known to play a role during fruit body formation. In terms of fruit body development, our analyses revealed a conserved repertoire of fruiting-related genes, which corresponds well to the archetypal fruit body morphology of this mushroom. For some genes involved in fruit body formation, paralogisation was observed, but not all fruit body maturation-associated genes known from other agaricomycetes seem to be conserved in the genome sequence of A. aegerita. In terms of lytic enzymes, our analyses suggest a versatile arsenal of biopolymer-degrading enzymes that likely account for the flexible life style of this species. Regarding the amount of genes encoding CAZymes relevant for lignin degradation, A. aegerita shows more similarity to white-rot fungi than to litter decomposers, including 18 genes coding for unspecific peroxygenases and three dye-decolourising peroxidase genes expanding its lignocellulolytic machinery.

Conclusions: The genome resource will be useful for developing strategies towards genetic manipulation of A. aegerita, which will subsequently allow functional genetics approaches to elucidate fundamentals of fruiting and vegetative growth including lignocellulolysis.

Keywords: Agaricales; Basidiomycetes; Carbohydrate active enzymes; Comparative genomics; Developmental biology; Fruit body; Mushroom; White-rot.

Fig. 1

Fruit body formation of A. aegerita AAE-3 on 2% malt extract agar after 10 days at 25 °C in the dark followed by incubation for 13 days at 20 °C in a 12 h light/12 h darkness regime (upper picture) or in the dark (lower picture). The scale bar represents 1 cm

Fig. 2

Putative homologs of agaricomycete fruiting-related genes in the genome of A. aegerita AAE-3 were identified by the basic local alignment search tool (BLAST; https://blast.ncbi.nlm.nih.gov/Blast.cgi) using published amino acid sequences of these genes from A. aegerita SM51 (=WT-1), Coprinopsis cinerea okayama7#130, C. cinerea AmutBmut pab1–1 and Schizophyllum commune H4–8 as query sequences (Additional file 6). Annotations of known functional elements and domains of the respective amino acid sequences were derived from InterProScan (http://www.ebi.ac.uk/interpro) and the NCBI Conserved Domain Database (CDD; https://www.ncbi.nlm.nih.gov/cdd). The scale bar represents 100 amino acids and the following abbreviations of domain names were used: ARID (AT-rich interaction domain) type DNA-binding domain; PAS (Per-Arnt-Sim) domain; HMG (high mobility group) box motif; FAD (flavin adenine dinucleotide); Fungal TF-MHR (transcription factor regulatory middle homology region)

Fig. 3

Distribution of the different CAZymes within the A. aegerita genome as obtained after HMMER search without (left) and with (right) an E-value threshold of 10⁻¹⁷. The following abbreviations were used: AA (auxiliary activity), CBM (carbohydrate-binding module), CE (carbohydrate esterase), GH (glycoside hydrolase), GT (glycosyl transferase) and PL (polysaccharide lyase)