Highly reduced complementary genomes of dual bacterial symbionts in the mulberry psyllid Anomoneura mori

Abstract

The genomes of obligately host-restricted bacteria suffer from accumulating mildly deleterious mutations, resulting in a drastic size reduction. Psyllids (Hemiptera) are phloem sap-sucking insects with a specialized organ called the bacteriome, which typically harbors two vertically transmitted bacterial symbionts: the primary symbiont "Candidatus Carsonella ruddii" (Gammaproteobacteria) and a secondary symbiont phylogenetically diverse among psyllid lineages. Genomes of several Carsonella lineages were revealed to be drastically reduced (158-174 kb), AT-rich (14.0-17.9% GC), and structurally conserved with similar gene inventories devoted for synthesizing essential amino acids scarce in the phloem sap. However, genomic information for secondary symbionts was limited. Hence, this study analyzed genomes of the bacteriome-associated dual symbionts, Secondary_AM (Gammaproteobacteria) and Carsonella_AM, in the mulberry psyllid Anomoneura mori (Psyllidae). This revealed that the Secondary_AM genome is as small and AT-rich (229,822 bp, 17.3% GC) as those of Carsonella, including Carsonella_AM (169,120 bp, 16.2% GC), implying that Secondary_AM is an evolutionarily ancient obligate mutualist like Carsonella. Phylogenomic analyses demonstrated that Secondary_AM is sister to "Candidatus Psyllophila symbiotica" of Cacopsylla spp. (Psyllidae), whose genomes (221-237 kb, 17.3-18.6% GC) were recently reported. The Secondary_AM and Psyllophila genomes showed highly conserved synteny, sharing all genes for complementing the incomplete tryptophan biosynthetic pathway of Carsonella and genes for synthesizing B vitamins. However, sulfur assimilation and carotenoid synthesizing genes were retained only in Secondary_AM and Psyllophila, respectively, indicating ongoing gene silencing. Average nucleotide identity, gene ortholog similarity, genome-wide synteny, and substitution rates suggested that the Secondary_AM/Psyllophila genomes are more labile than the Carsonella genomes.