Coexistence ofWolbachiawithBuchnera aphidicolaand a Secondary Symbiont in the AphidCinara cedri

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Abstract
Intracellular symbiosis is very common in the insect world. For the aphidCinara cedri, we have identified by electron microscopy three symbiotic bacteria that can be characterized by their different sizes, morphologies, and electrodensities. PCR amplification and sequencing of the 16S ribosomal DNA (rDNA) genes showed that, in addition to harboringBuchnera aphidicola, the primary endosymbiont of aphids,C. cedriharbors a secondary symbiont (S symbiont) that was previously found to be associated with aphids (PASS, or R type) and an α-proteobacterium that belongs to theWolbachiagenus. Using in situ hybridization with specific bacterial probes designed for symbiont 16S rDNA sequences, we have shown thatWolbachiawas represented by only a few minute bacteria surrounding the S symbionts. Moreover, the observedB. aphidicolaand the S symbionts had similar sizes and were housed in separate specific bacterial cells, the bacteriocytes. Interestingly, in contrast to the case for all aphids examined thus far, the S symbionts were shown to occupy a similarly sized or even larger bacteriocyte space thanB. aphidicola. These findings, along with the facts thatC. cedriharbors theB. aphidicolastrain with the smallest bacterial genome and that the S symbionts infect allCinaraspp. analyzed so far, suggest the possibility of bacterial replacement in these species.