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Somatic stem cell niche tropism in Wolbachia


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.


  1. 1

    Werren, J. H. & Windsor, D. M. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. Lond. B 267, 1277–1285 (2000)

    CAS  Article  Google Scholar 

  2. 2

    Jeyaprakash, A. & Hoy, M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9, 393–405 (2000)

    CAS  Article  PubMed  Google Scholar 

  3. 3

    Werren, J. H. & Bartos, J. D. Recombination in Wolbachia. Curr. Biol. 11, 431–435 (2001)

    CAS  Article  PubMed  Google Scholar 

  4. 4

    Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. & Bouletreau, M. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 16, 1711–1723 (1999)

    CAS  Article  PubMed  Google Scholar 

  5. 5

    O'Neill, S. L., Giordano, R., Colbert, A. M., Karr, T. L. & Robertson, H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl Acad. Sci. USA 89, 2699–2702 (1992)

    ADS  CAS  Article  PubMed  Google Scholar 

  6. 6

    Huigens, M. E., de Almeida, R. P., Boons, P. A., Luck, R. F. & Stouthamer, R. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. R. Soc. Lond. B 271, 509–515 (2004)

    CAS  Article  Google Scholar 

  7. 7

    Heath, B. D., Butcher, R. D., Whitfield, W. G. & Hubbard, S. F. Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr. Biol. 9, 313–316 (1999)

    CAS  Article  PubMed  Google Scholar 

  8. 8

    Grenier, S. et al. Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps. Proc. R. Soc. Lond. B 265, 1441–1445 (1998)

    Article  Google Scholar 

  9. 9

    Kang, L. et al. Superinfection of Laodelphax striatellus with Wolbachia from Drosophila simulans. Heredity 90, 71–76 (2003)

    CAS  Article  PubMed  Google Scholar 

  10. 10

    Rigaud, T., Pennings, P. S. & Juchault, P. Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. J. Invertebr. Pathol. 77, 251–257 (2001)

    CAS  Article  PubMed  Google Scholar 

  11. 11

    Zhang, Y. & Kalderon, D. Hedgehog acts as a somatic stem cell factor in the Drosophila ovary. Nature 410, 599–604 (2001)

    ADS  CAS  Article  PubMed  Google Scholar 

  12. 12

    Margolis, J. & Spradling, A. Identification and behaviour of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807 (1995)

    CAS  Google Scholar 

  13. 13

    Fuchs, E., Tumbar, T. & Guasch, G. Socializing with the neighbors: stem cells and their niche. Cell 116, 769–778 (2004)

    CAS  Article  Google Scholar 

  14. 14

    Ohlstein, B., Kai, T., Decotto, E. & Spradling, A. The stem cell niche: theme and variations. Curr. Opin. Cell Biol. 16, 693–699 (2004)

    CAS  Article  Google Scholar 

  15. 15

    Li, L. & Xie, T. Stem cell niche: structure and function. Annu. Rev. Cell. Dev. Biol. 21, 605–631 (2005)

    CAS  Article  PubMed  Google Scholar 

  16. 16

    Dobson, S. L. et al. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biol. 29, 153–160 (1999)

    CAS  Article  PubMed  Google Scholar 

  17. 17

    Min, K. T. & Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94, 10792–10796 (1997)

    ADS  CAS  Article  PubMed  Google Scholar 

  18. 18

    Cheng, Q. et al. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med. Vet. Entomol. 14, 44–50 (2000)

    CAS  Article  PubMed  Google Scholar 

  19. 19

    Mcgraw, E. A. & O'Neill, S. L. Wolbachia pipientis: intracellular infection and pathogenesis in Drosophila. Curr. Opin. Microbiol. 7, 67–70 (2004)

    CAS  Article  PubMed  Google Scholar 

  20. 20

    Hadfield, S. J. & Axton, J. M. Germ cells colonized by endosymbiotic bacteria. Nature 402, 482 (1999)

    ADS  CAS  Article  PubMed  Google Scholar 

  21. 21

    Veneti, Z., Clark, M. E., Karr, T. L., Savakis, C. & Bourtzis, K. Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl. Environ. Microbiol. 70, 5366–5372 (2004)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22

    Decotto, E. & Spradling, A. C. The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev. Cell 9, 501–510 (2005)

    CAS  Article  Google Scholar 

  23. 23

    Frydman, H. M. & Spradling, A. C. The receptor-like tyrosine phosphatase lar is required for epithelial planar polarity and for axis determination within Drosophila ovarian follicles. Development 128, 3209–3220 (2001)

    CAS  Google Scholar 

  24. 24

    Ferree, P. M. et al. Wolbachia utilizes host microtubules and dynein for anterior localization in the Drosophila oocyte. PLoS Pathogens 1, e14 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Mcgraw, E. A., Merritt, D. J., Droller, J. N. & O'Neill, S. L. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl Acad. Sci. USA 99, 2918–2923 (2002)

    ADS  CAS  Article  PubMed  Google Scholar 

  26. 26

    Lin, H. & Spradling, A. C. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol. 159, 140–152 (1993)

    CAS  Article  PubMed  Google Scholar 

  27. 27

    Clarkson, M. & Saint, R. A. His2AvDGFP fusion gene complements a lethal His2AvD mutant allele and provides an in vivo marker for Drosophila chromosome behaviour. DNA Cell Biol. 18, 457–462 (1999)

    CAS  Article  PubMed  Google Scholar 

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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 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).

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