Functional and Evolutionary Analysis of the Genome of an Obligate Fungal Symbiont

Nutritional symbionts of insects include some of the most bizarre genomes studied to date, with extremely reduced size, biased base composition, and limited metabolic abilities. A monophyletic group of aphids within the subfamily Cerataphidinae have lost the bacterial symbiont common to all other Aphididae (Buchnera aphidicola), which have been replaced by a eukaryotic one, the yeast-like symbiont (YLS). As symbionts are expected to experience reduced effective population size (N(e)) and largely clonal life cycles, we used this system as a model to test the hypothesis that chronically high levels of genetic drift will result in an increase in size of a eukaryotic genome. We sequenced the genome of the YLS of the aphid Cerataphis brasiliensis and observed elevated rates of protein sequence evolution and intron proliferation in YLS orthologs relative to those of its closest-sequenced relative, consistent with predictions. A moderate amount of repetitive DNA was found along with evidence of directed mutation to prevent proliferation of repetitive elements. Despite increased intron numbers, the overall genome structure appears not to have undergone massive expansion and is around 25 Mb in size. Compared with Buchnera, the YLS appears to have a much broader metabolic repertoire, though many gene families have been reduced in the YLS relative to related fungi. The patterns observed in the YLS genome suggest that its symbiotic lifestyle is permissive to intron proliferation and accelerated sequence evolution, though other factors appear to limit its overall genome expansion.