Secondary metabolite biosynthetic diversity in the fungal family Hypoxylaceae and Xylaria hypoxylon

Abstract

To date little is known about the genetic background that drives the production and diversification of secondary metabolites in the Hypoxylaceae . With the recent availability of high-quality genome sequences for 13 representative species and one relative ( Xylaria hypoxylon ) we attempted to survey the diversity of biosynthetic pathways in these organisms to investigate their true potential as secondary metabolite producers. Manual search strategies based on the accumulated knowledge on biosynthesis in fungi enabled us to identify 783 biosynthetic pathways across 14 studied species, the majority of which were arranged in biosynthetic gene clusters (BGC). The similarity of BGCs was analysed with the BiG-SCAPE engine which organised the BGCs into 375 gene cluster families (GCF). Only ten GCFs were conserved across all of these fungi indicating that speciation is accompanied by changes in secondary metabolism. From the known compounds produced by the family members some can be directly correlated with identified BGCs which is highlighted herein by the azaphilone, dihydroxynaphthalene, tropolone, cytochalasan, terrequinone, terphenyl and brasilane pathways giving insights into the evolution and diversification of those compound classes. Vice versa , products of various BGCs can be predicted through homology analysis with known pathways from other fungi as shown for the identified ergot alkaloid, trigazaphilone, curvupallide, viridicatumtoxin and swainsonine BGCs. However, the majority of BGCs had no obvious links to known products from the Hypoxylaceae or other well-studied biosynthetic pathways from fungi. These findings highlight that the number of known compounds strongly underrepresents the biosynthetic potential in these fungi and that a tremendous number of unidentified secondary metabolites is still hidden. Moreover, with increasing numbers of genomes for further Hypoxylaceae species becoming available, the likelihood of revealing new biosynthetic pathways that encode new, potentially useful compounds will significantly improve. Reaching a better understanding of the biology of these producers, and further development of genetic methods for their manipulation, will be crucial to access their treasures.

Fungal perylenequinones

“…A chemotaxonomic approach is required to substantiate the hypothesis that members of a specific family could produce PQs. A number of fascinating Hypoxylaceae chemotaxonomic studies have been achieved (Helaly et al 2018 ; Becker and Stadler 2021 ; Kuhnert et al 2021 ). They documented the occurrence of several secondary metabolites in Daldinia , Phylacia , Rhopalostroma , and Thamnomyces stromata, including ( 25 ).…”

Three New Species of Hypoxylon (Xylariales, Ascomycota) on a Multigene Phylogeny from Medog in Southwest China

“…Polyphasic taxonomic studies based on phylogenetic, chemotaxonomic, and morphological data were extensively applied to identify species and reflect evolutionary relationships of hypoxylaceous fungi in recent years [ 1 , 2 , 3 ]. Since resurrected and emended by Wendt et al [ 2 ], 15 genera were rearranged and recognized to Hypoxylaceae by having stromatal pigments and a nodulisporium-like anamorph.…”

Brunneosporopsis yunnanensis gen. et sp. nov. and Allocryptovalsa xishuangbanica sp. nov., New Terrestrial Sordariomycetes from Southwest China

“…Some taxa are fungicolous, while many persist as saprobes involved in decomposition and nutrient-recycling [ 6 , 8 ]. Some species of Sordariomycetes are economically important biocontrol agents, and others produce a wide range of chemically diverse metabolites important in agricultural, medicinal and other biotechnological industries [ 9 , 10 , 11 , 12 ].…”