Werth, S. | bioRxiv Science

bioRxiv2022

High diversity of type I polyketide genes in Bacidia rubella as revealed by the comparative analysis of 23 lichen fungal genomes

Fungi involved in lichen symbioses produce a large array of different secondary metabolites. The high diversity of those substances has been known for decades and are often considered characteristic for taxonomical delimitation in lichen-forming fungi. Polyketides, the most common secondary metabolites, are synthesized by the Type I Polyketide synthases (TI-PKS) comprised of different enzymatic domains. We present a phylogenetic overview of Type I PKS genes recovered from the de-novo sequenced genome of Bacidia rubella in the context of additional twenty-one fungal genomes from the largest radiation of lichen-forming Ascomycetes (Lecanoromycetes) as well as the lichen-forming Eurotiomycete, Endocarpon pusillum. Using de-novo gene prediction and functional annotation combined with a phylogenetic analysis, we provide insights into the biosynthetic potential and PKS gene diversity of lichen-forming fungi. We discuss genes predicted in the lichen-forming fungal genomes in relation to previously characterized PKS genes from other fungi and bacteria. Our results reveal a high number of biosynthetic gene clusters and their gene domain composition. PKS gene content outnumbers known secondary substances produced by the lichen-forming fungi. We were able to assign putative functions to several of those PKS genes in silico, based on similarity to already characterized genes. In particular, we identified a putative PKS23 gene of Bacidia rubella, producing the common lichen substance atranorin. However, we also found that several lichen-forming fungi still possess homologs of different biosynthetic genes without producing the corresponding substances in detectable amounts. Although many PKSs remain without functional assignments in our analysis, our findings highlight that genes from lichen-forming fungi represent an untapped source of novel polyketide compounds. However, additional experimental approaches are necessary to link biosynthetic genes and secondary metabolites with confidence.

evolutionary biology↗

bioRxiv2021

Large differences in carbohydrate degradation and transport potential in the genomes of lichen fungal symbionts

Lichen symbioses are generally thought to be stabilized by the transfer of fixed carbon compounds from a photosynthesizing unicellular symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with genomic reductions in the number of genes for plant cell wall-degrading enzymes (PCWDEs), but whether this is the case with lichen fungal symbionts (LFSs) is unknown. We predicted genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 17 existing and 29 newly sequenced genomes from across the class Lecanoromycetes, the largest extant clade of LFSs. Despite possessing lower mean numbers of PCWDE genes compared to non-symbiont Ascomycota, all LFS genomes possessed a robust suite of predicted PCWDEs. The largest CAZyme gene numbers, on par with model species such as Penicillium, were retained in genomes from the subclass Ostropomycetidae, which are found in crust lichens with highly specific ecologies. The lowest numbers were in the subclass Lecanoromycetidae, which are symbionts of many generalist macrolichens. Our results suggest that association with phototroph symbionts does not in itself result in functional loss of PCWDEs and that PCWDE losses may have been driven by adaptive processes within the evolution of specific LFS lineages. The inferred capability of some LFSs to access a wide range of carbohydrates suggests that some lichen symbioses may augment fixed CO2 with carbon from external sources. SignificanceLichen symbioses are considered self-contained autotrophic systems in which the total carbon economy is the sum of phototroph-fixed CO2, supplied to a fungus as sugars. In other fungal-plant symbioses, such as mycorrhizae, plant-derived sugar subsidies are associated with loss of plant cell wall-degrading enzymes (PCWDEs). We compared PCWDE inventories in 46 genomes from the largest group of lichen fungal symbionts (LFSs) with non-symbionts from across Ascomycota. We found that despite lower overall gene numbers, all LFSs retain PCWDEs, and some possess gene numbers and functional diversity on par with non-symbionts. Our results suggest that association with a phototroph does not necessarily result in PCWDE loss, and some lichens may obtain carbon from sources other than CO2 fixation.

genomics↗