New Clues about the Evolutionary History of Metabolic Losses in Bacterial Endosymbionts, Provided by the Genome of Buchnera aphidicola from the Aphid Cinara tujafilina

Abstract

ABSTRACT The symbiotic association between aphids (Homoptera) and Buchnera aphidicola ( Gammaproteobacteria ) started about 100 to 200 million years ago. As a consequence of this relationship, the bacterial genome has undergone a prominent size reduction. The downsize genome process starts when the bacterium enters the host and will probably end with its extinction and replacement by another healthier bacterium or with the establishment of metabolic complementation between two or more bacteria. Nowadays, several complete genomes of Buchnera aphidicola from four different aphid species ( Acyrthosiphon pisum , Schizaphis graminum , Baizongia pistacea , and Cinara cedri ) have been fully sequenced. C. cedri belongs to the subfamily Lachninae and harbors two coprimary bacteria that fulfill the metabolic needs of the whole consortium: B. aphidicola with the smallest genome reported so far and “ Candidatus Serratia symbiotica.” In addition, Cinara tujafilina , another member of the subfamily Lachninae, closely related to C. cedri , also harbors “ Ca. Serratia symbiotica” but with a different phylogenetic status than the one from C. cedri . In this study, we present the complete genome sequence of B. aphidicola from C. tujafilina and the phylogenetic analysis and comparative genomics with the other Buchnera genomes. Furthermore, the gene repertoire of the last common ancestor has been inferred, and the evolutionary history of the metabolic losses that occurred in the different lineages has been analyzed. Although stochastic gene loss plays a role in the genome reduction process, it is also clear that metabolism, as a functional constraint, is also a powerful evolutionary force in insect endosymbionts.