The evolution of lichen symbioses: A perspective from the genomics of the fungal symbiont (Supplementary files)

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. Using genomics, I explored lichen evolution across the phylum Ascomycota, from the perspectives of different fungal lineages, different photosynthetic symbionts, and their subsidy molecules. At the phylum level, I aim to resolve orphan links in ascomycotan evolution using genome profiling at high taxonomic levels. The resulting phylogenomic reconstruction of the ascomycotan tree of life showed that several orphan clades, together with six previously accounted classes, clustered into a single clade that includes multiple symbiotic lifestyles, such as lichens, mycorrhizae, and yeast-like symbionts in insect guts—currently circumscribed as Lichinomycetes. Using this updated phylogeny, I compared fungal genomes and found that lichen fungal genomes consistently had fewer functional annotations than other fungi, except for CAZymes. Moreover, the enzymatic machinery of lichen fungi 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 subsidy molecules: lichens subsidized by the polyol erythritol have larger enzymatic repertoires than those subsidized by glucose, sorbitol, or ribitol. These retained enzymes are primarily associated with carbon-harvesting functions, often streamlined as redundant functions in symbioses with a supplied carbon source. My results suggest that lichens may have more than one fate for their carbon subsidies, rather than solely operating as nutritional symbioses, driving distinct evolutionary paths. Finally, I explored lichen symbiosis using whole-evidence approaches, employing functionally unbiased orthogroups and machine-learning algorithms to identify genomic signatures that distinguish lichen fungi from non-lichen fungal genomes. Regardless of their different carbon-use profiles and lineage origins, lichen fungi share common genomic features that distinguish them from other fungi.Included here:Supplementary tables and filesChapter 2Chapter 3Chapter 4