Convergent evolution of metabolic roles in bacterial co-symbionts of insects

Abstract

A strictly host-dependent lifestyle has profound evolutionary consequences for bacterial genomes. Most prominent is a sometimes-dramatic amount of gene loss and genome reduction. Recently, highly reduced genomes from the co-resident intracellular symbionts of sharpshooters were shown to exhibit a striking level of metabolic interdependence. One symbiont, called Sulcia muelleri (Bacteroidetes), can produce eight of the 10 essential amino acids, despite having a genome of only 245 kb. The other, Baumannia cicadellinicola (gamma-Proteobacteria), can produce the remaining two essential amino acids as well as many vitamins. Cicadas also contain the symbiont Sulcia, but lack Baumannia and instead contain the co-resident symbiont Hodgkinia cicadicola (alpha-Proteobacteria). Here we report that, despite at least 200 million years of divergence, the two Sulcia genomes have nearly identical gene content and gene order. Additionally, we show that despite being phylogenetically distant and drastically different in genome size and architecture, Hodgkinia and Baumannia have converged on gene sets conferring similar capabilities for essential amino acid biosynthesis, in both cases precisely complementary to the pathways conserved in Sulcia. In contrast, they have completely divergent capabilities for vitamin biosynthesis. Despite having the smallest gene set known in bacteria, Hodgkinia devotes at least 7% of its proteome to cobalamin (vitamin B(12)) biosynthesis, a significant metabolic burden. The presence of these genes can be explained by Hodgkinia's retention of the cobalamin-dependent version of methionine synthase instead of the cobalamin-independent version found in Baumannia, a situation that necessitates retention of cobalamin biosynthetic capabilities to make the essential amino acid methionine.

Fig. 1.

Amino acid and vitamin-related gene contents of cicada and GWSS symbiont genomes. Abbreviations are Sm, Sulcia muelleri; Bc, Baumannia cicadellinicola; Hc, Hodgkinia cicadicola; and Ψ, pseudogene. Blue boxes represent amino acid biosynthesis genes that are present in a given genome, and green boxes represent vitamin biosynthesis genes. Note the pattern of conservation evident in amino acid biosynthesis genes but lacking in vitamin biosynthesis genes.

Fig. 2.

Genome conservation in cicada and GWSS Sulcia genomes. The cicada Sulcia genome is represented on the y axis and described in the top left box, and the GWSS Sulcia genome is represented on the x axis and described in the bottom right box. The red line indicates shared synteny between the two genomes. Gene names in the lower triangle are found in the GWSS Sulcia genome but not in the cicada Sulcia genome; gene names in the upper triangle are present in the cicada Sulcia genome but not in GWSS. Genes involved in replication, transcription, and translation are highlighted; aminoacyl tRNA synthetase genes are shown in yellow circles, and all others are shown in green boxes. Only named genes with clear functions were included in the figure for clarity; hypothetical genes, conserved hypothetical genes, and genes with ambiguous functions were omitted.

Fig. 3.

The aminoacyl tRNA synthetases and tRNAs found in cicada and GWSS symbiont genomes. Presence of an aminoacyl tRNA synthetase is indicated by shading in the column for each organism, light gray for GWSS symbionts and darker gray for cicada symbionts. The tRNAs that could be identified by computational methods are listed by anticodon sequences, and a parenthetical number indicates that many with an identical anticodon. Ellipses are shown for the second gene in a two component aminoacyl tRNA synthetase; refer to the box directly above for the relevant anticodon(s). ¹The tRNA-tryptophan in Hodgkinia is predicted to read both UGA and GGA codons because of the UGA Stop→Trp recoding in that genome (4). ²Hodgkinia has homologs of the gatA and gatB genes involved in generating tRNA-Gln from tRNA-Glu (44), potentially eliminating the need for glnS in this genome.