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

Abstract

AbstractThe 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 “CandidatusCarsonella ruddii” (Gammaproteobacteria) and a secondary symbiont phylogenetically diverse among psyllid lineages. Genomes of severalCarsonellalineages 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) andCarsonella_AM, in the mulberry psyllidAnomoneura mori(Psyllidae). This revealed that the Secondary_AM genome is as small and AT-rich (229,822 bp, 17.3% GC) as those ofCarsonella, includingCarsonella_AM (169,120 bp, 16.2% GC), implying that Secondary_AM is an evolutionarily ancient obligate mutualist likeCarsonella. Phylogenomic analyses demonstrated that Secondary_AM is sister to “CandidatusPsyllophila symbiotica” ofCacopsyllaspp. (Psyllidae), whose genomes (221–237 kb, 17.3–18.6% GC) were recently reported. The Secondary_AM andPsyllophilagenomes showed highly conserved synteny, sharing all genes for complementing the incomplete tryptophan biosynthetic pathway ofCarsonellaand genes for synthesizing B vitamins. However, sulfur assimilation and carotenoid synthesizing genes were retained only in Secondary_AM andPsyllophila, respectively, indicating ongoing gene silencing. Average nucleotide identity, gene ortholog similarity, genome-wide synteny, and substitution rates suggested that the Secondary_AM/Psyllophilagenomes are more labile than theCarsonellagenomes.