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The Drosophila-Spiroplasma interaction as a model to dissect the molecular mechanisms underlying insect endosymbiosis

Final Report Summary - DROSOSPIRO (The Drosophila-Spiroplasma interaction as a model to dissect the molecular mechanisms underlying insect endosymbiosis)

Virtually every species of insect harbors facultative bacterial endosymbionts that are transmitted from females to their offspring, often in the egg cytoplasm. These symbionts play crucial roles in the biology of their hosts. Many manipulate host reproduction in order to spread within host populations. Others increase the fitness of their hosts under certain conditions (for example by increasing tolerance to heat or by protecting their hosts against natural enemies). However, in spite of the growing interest in endosymbionts, very little is known about the molecular mechanisms underlying most endosymbiont-insect interactions. To fill this gap, we are dissecting the interaction between Drosophila and its native endosymbiont Spiroplasma poulsonii.
Our study has shown that S. poulsonii resides in large numbers in the hemolymph (the insect "blood") of larvae and adults. Surprisingly S. poulsonii cells are neither detected nor affected by the Drosophila immune system, but their proliferation is constrained by the availability of hemolymph lipids. We hypothesize that this dependence on lipids couples the proliferation of S. poulsonii to the nutritional state of its host. We have also provided strong evidences that the ability of Spiroplasma to protect Drosophila against infestation by parasitoid wasps (a parasite of Drosophila) relies on a competition for host lipids. Our study has also revealed that Spiroplasma uses the yolk uptake machinery to colonize the germ line, thus ensuring an efficient vertical transmission.
Spiroplasma is also a male killer (the male offspring of infected females dies during embryogenesis), and it has been hypothesized that this reproductive manipulation is one of the driving forces that maintains this facultative endosymbiont in fly populations. In collaboration with the Fukatsu lab, we have shown that Spiroplasma targets the dosage compensation system of Drosophila, a molecular machniery that is assembled only in males and that attaches to the X chromosome. Spiroplasma infection leads to DNA damage on the male X chromosome (formation of chromatin bridges during mitosis) that causes later apoptosis via the p53-dependent pathway. More recently, we have identified the Spiroplasma gene that mediates male killing sovlign a mystery of more than 50 years.
Our laboratory has also recently sequenced the genome of S. poulsonii and developped new approaches to cultivate it in vitro and transform it. These works pave the route to the genetic manipulation of this symbiont.
We believe that the fundamental knowledge generated on the Drosophila-Spiroplasma interaction will serve as a paradigm for other endosymbiont-insect interactions (ex. Wolbachia) that are less amenable to genetic studies.