Evidence of ancient horizontal gene transfer between fungi and the terrestrial alga Trebouxia

Intimate and long-lasting relationships of fungi and algae have been known for centuries by scientists, and these ancient symbioses might have provided excellent opportunities for horizontal gene transfer (HGT) of protein encoding genes between the two organismal partners. In this study, we sequenced and assembled 451 Mbp of novel genomic DNA from Trebouxia decolorans (Trebouxiaceae, Chlorophyta), the green algal photobiont of the lichen Xanthoria parietina (Teloschistaceae, Lecanoromycetes, Ascomycota). This alga also occurs as a free-living terrestrial organism. The aim of our work was to search for candidate genes pointing to HGT between lichenized fungi and lichen algae. We found evidence for three putative HGT events of fungal genes into the Trebouxia genome, but these are likely more ancient (over 600 mya) than the origin of lichenization within the fungal Ascomycetes. The three transferred genes are part of gene groups that in other species encode a tellurite-resistance dicarboxylate transporter (TDT) family protein, a class-1 nitrilase/cyanide hydratase (CH), and an oxidoreductase/retinol dehydrogenase. In each case, our phylogenomic analyses show orthologs from Trebouxia as sister to orthologs from all fungi or basally placed within Ascomycetes, while the orthologs from green algae and land plants form separate, independent evolutionary lineages. Alternative hypothesis tests significantly support these HGT events. The presence of these genes in Trebouxia was validated by PCR amplification of separately isolated Trebouxia DNA. The ancient incorporation of fungal genes in the genomes of these particular green algae are intriguing and could be early evidence for symbiotic and co-evolutionary relationships among the major eukaryotic branches of algae and fungi present in early terrestrial life on Earth. These genes could have played a pre-disposition role for some fungi and algae in the origin of lichen symbiosis, but further studies are needed to evaluate this in detail.