Tsuchida, Tsutomu

ABSTRACT Members of the genus Rickettsiella are bacterial pathogens of insects and other arthropods. Recently, a novel facultative endosymbiont, “ Candidatus Rickettsiella viridis,” was described in the pea aphid Acyrthosiphon pisum , whose infection causes a striking host phenotype: red and green genetic color morphs exist in aphid populations, and upon infection with the symbiont, red aphids become green due to increased production of green polycyclic quinone pigments. Here we determined the complete genome sequence of the symbiont. The 1.6-Mb circular genome, harboring some 1,400 protein-coding genes, was similar to the genome of entomopathogenic Rickettsiella grylli (1.6 Mb) but was smaller than the genomes of phylogenetically allied human pathogens Coxiella burnetii (2.0 Mb) and Legionella pneumophila (3.4 Mb). The symbiont’s metabolic pathways exhibited little complementarity to those of the coexisting primary symbiont Buchnera aphidicola , reflecting the facultative nature of the symbiont. The symbiont genome harbored neither polyketide synthase genes nor the evolutionarily allied fatty acid synthase genes that are suspected to catalyze the polycyclic quinone synthesis, indicating that the green pigments are produced not by the symbiont but by the host aphid. The symbiont genome retained many type IV secretion system genes and presumable effector protein genes, whose homologues in L. pneumophila were reported to modulate a variety of the host's cellular processes for facilitating infection and virulence. These results suggest the possibility that the symbiont is involved in the green pigment production by affecting the host’s metabolism using the secretion machineries for delivering the effector molecules into the host cells. IMPORTANCE Insect body color is relevant to a variety of biological aspects such as species recognition, sexual selection, mimicry, aposematism, and crypsis. Hence, the bacterial endosymbiont “ Candidatus Rickettsiella viridis,” which alters aphid body color from red to green, is of ecological interest, given that different predators preferentially exploit either red- or green-colored aphids. Here we determined the complete 1.6-Mb genome of the symbiont and uncovered that, although the red-green color transition was ascribed to upregulated production of green polycyclic quinone pigments, the symbiont genome harbored few genes involved in the polycyclic quinone biosynthesis. Meanwhile, the symbiont genome contained type IV secretion system genes and presumable effector protein genes, whose homologues modulate eukaryotic cellular processes for facilitating infection and virulence in the pathogen Legionella pneumophila . We propose the hypothesis that the symbiont may upregulate the host’s production of polycyclic quinone pigments via cooption of secretion machineries and effector molecules for pathogenicity.

ABSTRACTA gammaproteobacterial facultative symbiont of the genusRickettsiellawas recently identified in the pea aphid,Acyrthosiphon pisum. Infection with this symbiont altered the color of the aphid body from red to green, potentially affecting the host's ecological characteristics, such as attractiveness to different natural enemies. In European populations ofA. pisum, the majority ofRickettsiella-infected aphids also harbor another facultative symbiont, of the genusHamiltonella. We investigated thisRickettsiellasymbiont for its interactions with the coinfectingHamiltonellasymbiont, its phenotypic effects onA. pisumwith and withoutHamiltonellacoinfection, and its infection prevalence inA. pisumpopulations. Histological analyses revealed that coinfectingRickettsiellaandHamiltonellaexhibited overlapping localizations in secondary bacteriocytes, sheath cells, and hemolymph, whileRickettsiella-specific localization was found in oenocytes.Rickettsiellainfections consistently altered hosts' body color from red to green, where the greenish hue was affected by both host and symbiont genotypes.Rickettsiella-Hamiltonellacoinfections also changed red aphids to green; this greenish hue tended to be enhanced byHamiltonellacoinfection. With different host genotypes,Rickettsiellainfection exhibited either weakly beneficial or nearly neutral effects on host fitness, whereasHamiltonellainfection andRickettsiella-Hamiltonellacoinfection had negative effects. Despite considerable frequencies ofRickettsiellainfection in European and North AmericanA. pisumpopulations, noRickettsiellainfection was detected among 1,093 insects collected from 14 sites in Japan. On the basis of these results, we discuss possible mechanisms for the interaction ofRickettsiellawith other facultative symbionts, their effects on their hosts' phenotypes, and their persistence in natural host populations. We propose the designation “CandidatusRickettsiella viridis” for the symbiont.