Basidiospores from Wood-Decay Fungi Transform Laccase Substrates in the Absence of Glucose and Nitrogen Supplements

Abstract

Preparations of bacterial endospores and fungal conidia are applied in biocontrols, biocatalyses, and lignocellulose fermentations. The biocatalytic abilities of basidiospores from mushrooms of the order Agaricales are unknown. To assess their potential in colonizing recalcitrant substrates solely with their inherent resources, spores of the white-rot fungi Stropharia rugoso-annulata (Stru) and Kuehneromyces mutabilis (Kmt, Strophariaceae) were analyzed for surface-bound and internal total carbohydrates, phenols, proteins, minerals, and oxidoreductases to estimate their chemistry and the preconditions to transform the laccase substrates guaiacol and 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS) independent of external glucose and nitrogen. Surfaces of Stru/Kmt spores released (mg kg−1) hexoses, 7300/9700; phenols, >62/220; proteins, 21/168; and laccases, 42/0–0.15 µmol ABTS•+ kg−1 min−1 that mimicked oxidative activities of the resting spores. Milled-spore extracts contained pentoses, 96,600/6750; hexoses, 160,000/15,130; phenols, 452/767; protein, 12,600/924; true laccase, 688/0.30; and enzyme-protein-activating transition metals such as Cu in concentrations typical of wheat grains. Independent of external N and C supply, spores (<1‰) germinated in bideionized water, supported by their surface resources. Kmt spores germinated, too, at comparable rates in N-free solutions of glucose and the not immediately metabolizable ABTS and guaiacol. The release of proteins and oxidoreductase(s) by Kmt spores starting upon germination was higher in guaiacol-incubated idiophase- than in glucose-incubated trophophase-spores and led to the 3–4-fold formation of guaiacol polymerizates and ABTS•+. Constitutive aromatic ring-cleaving dioxygenases in the dormant spore that could be involved in the intrinsic metabolization of guaiacol were not detected. It is concluded that intrinsic resources enable (germinating) spores to release the highly efficient laccases of basidiomycetes and to transform aromatic compounds in the absence of sugar amendments. Spores show therefore plant seed-like autonomy in nutrient modification and acquisition during the early stages of the colonization of inert substrates.

Genomic Analysis of Stropharia rugosoannulata Reveals Its Nutritional Strategy and Application Potential in Bioremediation

“…Cultivation substrates include both cellulosic straw and lignin sawdust. Most studies have considered it an LD [9,16]; however, some reports have classified it as a WR [17,18]. It has been reported that LD fungi shares with WR fungi the plesiomorphic enzymatic network involved in cellulose decomposition, whereas genomic signatures related to hemicellulose-and lignin-degradation genes can separate LD fungi from most WR fungi [25].…”

“…From an ecophysiological point of view, saprotrophic basidiomycetes can be classified into three partially overlapping groups, namely, brown rot (BR), white rot (WR), and litterdecomposing (LD) fungi. S. rugosoannulata can assimilate both cellulosic straw and lignin sawdust; it is categorized as LD [9,16] or WR [17,18]. This is different from a typical LD, such as Agaricus bispora, which is usually cultivated on wheat and rice straw.…”