Abstract
Lichen-forming fungi produce a vast number of unique natural products with a wide variety of biological activities and human uses. Although lichens have remarkable potential in natural product research and industry, the molecular mechanisms underlying the biosynthesis of lichen metabolites are poorly understood. Here we use genome mining and comparative genomics to assess biosynthetic gene clusters and their putative regulators in the genomes of two lichen-forming fungi, which have substantial commercial value in the perfume industry, Evernia prunastri and Pseudevernia furfuracea. We report a total of 80 biosynthetic gene clusters (polyketide synthases (PKS), non-ribosomal peptide synthetases and terpene synthases) in E. prunastri and 51 in P. furfuracea. We present an in-depth comparison of 11 clusters, which show high homology between the two species. A ketosynthase (KS) phylogeny shows that biosynthetic gene clusters from E. prunastri and P. furfuracea are widespread across the Fungi. The phylogeny includes 15 genomes of lichenized fungi and all fungal PKSs with known functions from the MIBiG database. Phylogenetically closely related KS domains predict not only similar PKS architecture but also similar cluster architecture. Our study highlights the untapped biosynthetic richness of lichen-forming fungi, provides new insights into lichen biosynthetic pathways and facilitates heterologous expression of lichen biosynthetic gene clusters.
Highlights
Lichens are symbioses, composed of a fungal partner and one or more photosynthetic partners [1]
We address the following questions: What is the diversity of biosynthetic gene clusters in Evernia prunastri and Pseudevernia furfuracea and how does it compare to other lichenized fungi and non-lichenized fungi?
Pseudevernia furfuracea and especially E. prunastri show a high number of biosynthetic gene clusters (Table 2), and a high number of natural products has been reported for both species [25,26]
Summary
Lichens are symbioses, composed of a fungal partner (mycobiont) and one or more photosynthetic partners (photobiont) [1]. For the prediction of biosynthetic function of PKS genes there are diverse strategies, apart from experimental evidence through gene knockout, heterologous expression, radiolabelling or oxidation experiments [48,49,50,51] These include phylogenetic approaches to infer the functions through a close phylogenetic relatedness to characterized genes [52,53], transcriptional profiling [43,47], or comparative homology mapping of entire gene clusters [31,36,54]. The secondary metabolite richness and partially overlapping chemical profiles make these species interesting study systems for combining genome mining and comparative genomics to investigate biosynthetic enzymes that may be responsible for the production of characteristic lichen substance classes. (III) Where do PKSs from E. prunastri and P. furfuracea group phylogenetically in a phylogeny of PKSs with known functions?
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