Carbohydrate degradation machineries in lichen fungal symbionts reveal distinct symbiotic footprints across Ascomycota

Abstract

Lichens--the archetypal symbiosis--have long been known for their nutritional relationship, in which the photoautotrophic partners subsidize the carbon needs of their fungal symbiont. Yet, this subsidiary framing obscures the fact that lichenization has evolved multiple times across different fungal lineages and involves a wide array of phylogenetically distinct photosynthetic symbionts and subsidy types. Here, we compiled and functionally annotated 309 fungal genomes--including 24 newly generated metagenomically assembled genomes--with 191 representing lichen fungal symbionts spanning all taxonomic classes with lichen symbioses in Ascomycota. We found that lichen fungal genomes consistently had fewer annotations than other fungi, except for CAZymes. Moreover, the enzymatic machinery of lichen fungal symbionts exhibits a distinct bimodal pattern, with some genomes maintaining large enzymatic repertoires, while others hold some of the smallest sets in ascomycotan fungi. This pattern closely aligns with their photobiont subsidiary molecules; lichens subsidized by their photobiont with the polyol erythritol possess large enzymatic repertoires compared to those that receive glucose, sorbitol, or ribitol. These retained enzymes are primarily related to carbon-harvesting functions, often streamlined as redundant functionalities in symbioses with a supplied carbon source. Our results suggest that lichens may have more than one fate for their carbon subsidies, rather than solely operating as nutritional symbioses.