Genome Evolution of the Obligate Endosymbiont Buchnera aphidicola

Abstract

Abstract An evolutionary consequence of uniparentally transmitted symbiosis is degradation of symbiont genomes. We use the system of aphids and their maternally inherited obligate endosymbiont, Buchnera aphidicola, to explore the evolutionary process of genome degradation. We compared complete genome sequences for 39 Buchnera strains, including 23 newly sequenced symbiont genomes from diverse aphid hosts. We reconstructed the genome of the most recent shared Buchnera ancestor, which contained 616 protein-coding genes, and 39 RNA genes. The extent of subsequent gene loss varied across lineages, resulting in modern genomes ranging from 412 to 646 kb and containing 354–587 protein-coding genes. Loss events were highly nonrandom across loci. Genes involved in replication, transcription, translation, and amino acid biosynthesis are largely retained, whereas genes underlying ornithine biosynthesis, stress responses, and transcriptional regulation were lost repeatedly. Aside from losses, gene order is almost completely stable. The main exceptions involve movement between plasmid and chromosome locations of genes underlying tryptophan and leucine biosynthesis and supporting nutrition of aphid hosts. This set of complete genomes enabled tests for signatures of positive diversifying selection. Of 371 Buchnera genes tested, 29 genes show strong support for ongoing positive selection. These include genes encoding outer membrane porins that are expected to be involved in direct interactions with hosts. Collectively, these results indicate that extensive genome reduction occurred in the ancestral Buchnera prior to aphid diversification and that reduction has continued since, with losses greater in some lineages and for some loci.