Defensive Bacteriome Symbiont with a Drastically Reduced Genome

Diverse insect species harbor symbiotic bacteria, which play important roles such as provisioning nutrients and providing defense against natural enemies. Whereas nutritional symbioses are often indispensable for both partners, defensive symbioses tend to be of a facultative nature. The Asian citrus psyllid Diaphorina citri is a notorious agricultural pest that transmitsLiberibacter spp. (Alphaproteobacteria), causing the devastating citrus greening disease or Huanglongbing. In a symbiotic organ called the bacteriome, D. citri harbors two distinct intracellular symbionts: a putative nutrition provider, Carsonella_DC (Gammaproteobacteria), and an unnamed betaproteobacterium with unknown function, for which we propose the name “Candidatus Profftella armatura.” Here we report that Profftella is a defensive symbiont presumably of an obligate nature with an extremely streamlined genome. The genomes of Profftella and Carsonella_DC were drastically reduced to 464,857 bp and 174,014 bp, respectively, suggesting their ancient and mutually indispensible association with the host. Strikingly, 15% of the small Profftella genome encoded horizontally acquired genes for synthesizing a novel polyketide toxin. The toxin was extracted, pharmacologically and structurally characterized, and designated diaphorin. The presence of Profftella and its diaphorin-biosynthetic genes was perfectly conserved in the world’s D. citri populations.