Lichenization, the symbiosis of a fungus with photosynthesizing alga or cyanobacteria is a highly successful lifestyle. It allows lichens to conquer ecological niches that are otherwise too extreme to support eukaryotic life. Most lichenized fungi are members of the Lecanoromycetes, accounting for about half of the so far described ascomycetes. Their degree of dependence on their symbiotic partner varies and has in many instances evolved to an extent that the respective fungus grow very poorly – if at all – in isolation. This renders lichen communities excellent examples to study the genomic footprint of the evolutionary process turning an autonomously living organism into an obligate symbiont. However, the data acquisition itself is a challenge. For lichens growing poorly in culture, the only feasible method of genome analysis is the metagenomic sequencing of the eukaryotic and bacterial components.
Building on a benchmarking study about potentials and pitfalls of lichen metagenomics, we here present the first high-quality genomes of a lichenized fungus, Lasallia pustulata, and its photobiont, Trebouxia sp., generated purely from metagenomic samples. We compared the genome of Lasallia pustulata to two cultureable Lecanoromycetes, Cladonia grayi and Xanthoria parietina, and further 18 non-lichenized Pezizomycetes. This revealed a pronounced loss of otherwise highly conserved pezizomycete core-genes specifically on the lineage of L. pustulata. We confirmed the absence of these through gene order analyses. Their functional annotation through KEGG showed a widespread loss of metabolic capacity in L. pustulata across all metabolic pathways. This metabolic reduction can be at least partially mitigated by the bacterial communities present in L. pustulata, as metagenomic samples collected from a wide geographic range, showed a stable core-set of bacteria and metabolic functions across those. We conclude that lichenization enables reductive evolution in the individual symbionts, potentially made possible by the genomic redundancy across the lichen hologenome.