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

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.

Fig. 1.

Maximum likelihood (ML) phylogeny inferred from the 310 concatenated gene sequences shared by Buchnera strains and E. coli (Eco). The support values for the corresponding inner branch are 100/1.0 in the form of the proportion of bootstrap pseudoreplicates/Bayesian a posteriori probabilities, respectively. The total numbers of genes of each strain, as well as in the last common symbiotic ancestor (LCSA), are indicated in gray boxes. Numbers within squares at the nodes indicate the total number of gene losses. B. aphidicola strain abbreviations are as explained in Table 1, footnote b.

Fig. 2.

Evolutionary diagram of metabolic gene losses occurring in the five strains of B. aphidicola since the LCSA. The inferred pathways that had already been lost in the LCSA are indicated in the large gray rounded box in the top left corner of the figure. The small shadowed boxes show the number of total gene losses/number of gene losses involved in metabolism in each lineage. The adjacent boxes to the right of the lineages indicated only the new metabolic pathways affected by these gene losses. B. aphidicola strains are abbreviated as explained in Table 1, footnote b. CoA, coenzyme A; AICAR, amino-imidazole carboxamide riboside 5′-phosphate; SAM, S-adenosylmethionine.

Fig. 3.

Phylogenetic representation of gene loss events in each Buchnera strain for repair machinery. B. aphidicola strains are abbreviated as explained in Table 1, footnote b.