A basidomycetous hydroxynaphthalene-prenylating enzyme exhibits promiscuity toward prenyl donors

Abstract

The fungal prenyltransferase ShPT from Stereum hirsutum was believed to prenylate 4-hydroxybenzyl alcohol and thereby be involved in the vibralactone biosynthesis. In this study, we demonstrate that hydroxynaphthalenes instead of benzyl alcohol or aldehyde were accepted by ShPT for regular C-prenylation in the presence of both dimethylallyl and geranyl diphosphate. Although the natural substrate of ShPT remains unknown, our results provide one additional prenyltransferase from basidiomycetes, which are less studied, in comparison to those from other sources. Furthermore, this study expands the chemical toolbox for regioselective production of prenylated naphthalene derivatives. Key points •Basidiomycetous prenyltransferase •Biochemical characterization •A DMATS prenyltransferase prenylating hydroxynaphthalene derivatives

Parallel Evolution of Asco- and Basidiomycete O-Prenyltransferases

“…Both genomes share a nearly identical gene encoding a DMATS-type PT (LaTyrPT and LbTyrPT, 93.5% similarity) that may represent candidates for a potential O -prenylating PT (Table S1). In a comprehensive phylogenetic analysis, these two Laccaria PTstogether with the characterized basidiomycete DMATS-like PTs BypB and ShPT known to prenylate phenolic compoundsform a particular novel clade of basidiomycete DMATS-like PTs that evolved independently from the DMATS counterparts in Ascomycota as supported by a high bootstrap value (96%, Figure , Figure S1). Moreover, the data suggest that ascomycete aryl-prenylating PTs known to modify phenolic polyketides may have evolved from tyrosine PTs.…”

“…3 Characterized DMATS-type enzymes are the C-prenylating BypB for cloquetin assembly, 10 Vib-PT that catalyzes C-prenylation of 4-hydroxybenzaldehyde and O-prenylation of 4-hydroxybenzylalcohol, 11 and ShPT that C-prenylates naphthalene derivatives. 12 More basidiomycete O-prenylating PTs have surprisingly not been identified yet, contrasting 35 PTs known from ascomycetes. 8 However, a wide variety of O-prenylated compounds have been isolated from basidiomycetes, e.g., the serpulanins from Serpula spp., 13 some strobilurins from Agaricales, 14 multiple benzaldehydeand benzofuran-derived compounds 15 from Russulales, dozens of tyrosinyl succinimides 16 from Antrodia spp., and the 3-(3methylbut-2-enyloxy)-4-O-α-D-ribofuranose benzoic acid methyl ester riboside from Laccaria species (the deceiver mushrooms) 17 (Figure 1).…”

“…While numerous prenylated compounds from basidiomycetes have been isolated and structurally characterized, only a single-digit number of PTs have been functionally characterized, including the UbiA-type PTs VibP1 and VibP2 for vibralactone biosynthesis . Characterized DMATS-type enzymes are the C-prenylating BypB for cloquetin assembly, Vib-PT that catalyzes C -prenylation of 4-hydroxybenzaldehyde and O -prenylation of 4-hydroxybenzylalcohol, and ShPT that C -prenylates naphthalene derivatives . More basidiomycete O -prenylating PTs have surprisingly not been identified yet, contrasting 35 PTs known from ascomycetes .…”