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Somatic stem cell niche tropism in Wolbachia

Abstract

Wolbachia are intracellular bacteria found in the reproductive tissue of all major groups of arthropods1,2. They are transmitted vertically from the female hosts to their offspring, in a pattern analogous to mitochondria inheritance. But Wolbachia phylogeny does not parallel that of the host, indicating that horizontal infectious transmission must also occur3,4,5. Insect parasitoids are considered the most likely vectors, but the mechanism for horizontal transfer is largely unknown4,6,7. Here we show that newly introduced Wolbachia cross several tissues and infect the germline of the adult Drosophila melanogaster female. Through investigation of bacterial migration patterns during the course of infection, we found that Wolbachia reach the germline through the somatic stem cell niche in the D. melanogaster germarium. In addition, our data suggest that Wolbachia are highly abundant in the somatic stem cell niche of long-term infected hosts, implying that this location may also contribute to efficient vertical transmission. This is, to our knowledge, the first report of an intracellular parasite displaying tropism for a stem cell niche.

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Figure 1: Wolbachia introduced in the abdominal cavity reaches the germline.
Figure 2: Wolbachia preferentially infect the somatic stem cell niche (SSCN).
Figure 3: Wolbachia at the abdominal cavity of maternally infected flies infect newly introduced germarium.

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Acknowledgements

We thank G. Deshpande, T. Schupbach and A. Nouri for comments on the manuscript; A. Spradling, D. D. Barbosa, P. Ferree and W. Sullivan for stocks and reagents; B. Burdine for help with injection experiments; J. Goodhouse for microscopy assistance; and A. Basile, and the Wieschaus and Schupbach laboratory members for support during the realization of this work. Author Contributions H.M.F. planned the project. H.M.F. and E.W. designed experiments. H.M.F. and J.M.L. performed experiments. D.N.R. wrote the image analysis software and statistical analysis. H.F. and E.W. contributed reagents and materials. H.M.F. wrote the paper. E.W., D.N.R. and J.M.L. edited the paper.

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Correspondence to Horacio M. Frydman.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Figures 1 and 2, Supplementary Table 1, Supplementary Methods and Supplementary Video Legend. This file also contains additional references. (PDF 2145 kb)

Supplementary Video

Volumetric reconstruction from confocal microscopy of the germarium with a single infected SSCN. This movie shows a rotation of this germarium, allowing comparison of the levels of Wolbachia in the follicle cells between the infected and the uninfected sides. (MOV 3269 kb)

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Frydman, H., Li, J., Robson, D. et al. Somatic stem cell niche tropism in Wolbachia. Nature 441, 509–512 (2006). https://doi.org/10.1038/nature04756

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