Genome sequence of the button mushroomAgaricus bisporusreveals mechanisms governing adaptation to a humic-rich ecological niche

Abstract

Agaricus bisporus is the model fungus for the adaptation, persistence, and growth in the humic-rich leaf-litter environment. Aside from its ecological role, A. bisporus has been an important component of the human diet for over 200 y and worldwide cultivation of the “button mushroom” forms a multibillion dollar industry. We present two A. bisporus genomes, their gene repertoires and transcript profiles on compost and during mushroom formation. The genomes encode a full repertoire of polysaccharide-degrading enzymes similar to that of wood-decayers. Comparative transcriptomics of mycelium grown on defined medium, casing-soil, and compost revealed genes encoding enzymes involved in xylan, cellulose, pectin, and protein degradation are more highly expressed in compost. The striking expansion of heme-thiolate peroxidases and β-etherases is distinctive from Agaricomycotina wood-decayers and suggests a broad attack on decaying lignin and related metabolites found in humic acid-rich environment. Similarly, up-regulation of these genes together with a lignolytic manganese peroxidase, multiple copper radical oxidases, and cytochrome P450s is consistent with challenges posed by complex humic-rich substrates. The gene repertoire and expression of hydrolytic enzymes in A. bisporus is substantially different from the taxonomically related ectomycorrhizal symbiont Laccaria bicolor . A common promoter motif was also identified in genes very highly expressed in humic-rich substrates. These observations reveal genetic and enzymatic mechanisms governing adaptation to the humic-rich ecological niche formed during plant degradation, further defining the critical role such fungi contribute to soil structure and carbon sequestration in terrestrial ecosystems. Genome sequence will expedite mushroom breeding for improved agronomic characteristics.

Lentinula edodes Genome Survey and Postharvest Transcriptome Analysis

“…The resulting scaffold number was 1,951, the N 50 was 103,018, and the total was 38,944,209 bp (see Table S1 in the supplemental material). The resulting scaffolds were comparable with those from other genome sequence data from mushroom-forming basidiomycetous fungal species, such as from Coprinopsis cinerea (37 Mb) (10), Agaricus bisporus (30 Mb) (11), and Schizophyllum commune (38.5 Mb) (12), but were smaller than that from the mycorrhizal basidiomycetous fungus Laccaria bicolor (65 Mb) (9). Previously, we carried out gene prediction by draft genome sequencing of Lentinula edodes strain D703PP-9 and found 8,271 putative genes (25).…”

“…Genome sequence data have been published for basidiomycetous fungi such as Phanerochaete chrysosporium (8), Laccaria bicolor (9), Coprinopsis cinerea (10), Agaricus bisporus (11), Schizophyllum commune (12), and Flammulina velutipes (13). Because of the popularity of next-generation sequencing, many genome sequence drafts of basidiomycetous fungi are publicly available, especially from the 1,000 Fungal Genomes Project (14).…”

“…Some transcriptome analyses with genome sequence data have been reported in several mushrooms, such as Agaricus bisporus (11), Schizophyllum commune (12), and others. Transcriptome analyses for fruiting body development in Lentinula edodes were carried out using differential display (17) or serial analysis of gene expression (SAGE) analysis (18), and PCR subtraction was used for analyzing postharvest quality loss (19).…”

Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi

“…This diverse phylum includes the mushrooms (12)(13)(14); pathogens of plants (2), animals (9)(10)(11), and other fungi (15); osmotically tolerant molds (16); ectomycorrhizal symbionts like Laccaria bicolor, which are critical for plant growth; plant pathogens, such as rusts and smuts (7); and saprotrophs, including wood-decaying fungi (17).…”

“…Agaricomycotina includes many decomposers of wood and leaf litter (12,17,(20)(21)(22)(23)) that produce lignocellulolytic enzymes that have potential to be used in bioenergy production (24)(25)(26)(27). Thus, much of sequencing effort at the US Department of Energy (DOE) Joint Genome Institute (JGI) (http://jgi.doe.gov/fungi) has targeted Agaricomycotina, particularly the Agaricomycetes (mushroom-forming fungi), with the large orders Agaricales (predominantly gilled mushrooms), Polyporales (wood-decaying polypores and others), and Boletales (porcini mushrooms and others) being especially deeply sampled.…”