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

Abstract

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.