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.

Evolutionary biology of lichen symbioses

“…Resl et al . (2022) compared PCWDE richness in 49 lichen fungal genomes in the class Lecanoromycetes to related nonsymbiont clades of Ascomycota . They found that PCWDE richness does not neatly correlate with fungal association with an alga.…”

“…They found that PCWDE richness does not neatly correlate with fungal association with an alga. In some lineages, PCWDEs are reduced compared to nonsymbionts, but in others, PCWDE diversity is on par with model saprotrophs such as Aspergillus (Resl et al ., 2022). Furthermore, Resl et al .…”

“…Furthermore, Resl et al . (2022) recovered a putative invertase ortholog in all studied lichen fungi. These results are consistent with experimental evidence over several decades that lichen fungi possess functional cellulases, oxidoreductases and pectinases (reviewed by Beckett et al ., 2013) as well as invertases (Fahselt, 1994).…”

“…Resl et al . (2022) suggested that evolutionary feedback loops subsequent to the origin of the symbiosis, such as the evolution of complex lichen traits, could have impacted PCWDEs in specific lineages (see Section VII). Comparable studies of genomic signatures of anhydrobiosis have yet to be carried out.…”

“…These results are consistent with experimental evidence over several decades that lichen fungi possess functional cellulases, oxidoreductases and pectinases (reviewed by Beckett et al, 2013) as well as invertases (Fahselt, 1994). Resl et al (2022) suggested that evolutionary feedback loops subsequent to the origin of the symbiosis, such as the evolution of complex lichen traits, could have impacted PCWDEs in specific lineages (see Section VII). Comparable studies of genomic signatures of anhydrobiosis have yet to be carried out.…”