Skip to main content
Log in

Closely Related Wolbachia Strains within the Pumpkin Arthropod Community and the Potential for Horizontal Transmission via the Plant

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Phylogenetic studies have implicated frequent horizontal transmission of Wolbachia among arthropod host lineages. However, the ecological routes for such lateral transfer are poorly known. We surveyed the species of two arthropod communities, one on pumpkin and the other on loofah plants, for Wolbachia, constructed wsp gene phylogenies of those Wolbachia strains found to infect community members, and established ecological links among infected members. Four taxonomically diverse insects in the pumpkin arthropod community contained very closely related Wolbachia wsp sequences (<1.5% divergence by Kimura-2-parameter distances). These insects, namely, the whitefly Bemisia tabaci, the planthopper Nisia nervosa, the flea beetle Phyllotreta sp., and the fleahopper Halticus minutus, were all collected from pumpkin leaves. They were ecologically linked through feeding on the same leaf substrate. Unlike other infected leaf insects, the whitefly population appeared to have a permanent breeding relationship with pumpkin plants, and high and stable, but not fixed, monthly Wolbachia infection rates. Our findings suggest potential roles for the plant in Wolbachia transmission and for whiteflies in being an infection source for other pumpkin leaf-feeding insects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Bordenstein, SR, Wernegreen, JJ (2004) Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol 21: 1981–1991

    Article  PubMed  CAS  Google Scholar 

  2. Cook, J, Butcher, R (1999) The transmission and effects of Wolbachia bacteria in parasitoids. Res Pop Ecol 41: 15–28

    Article  Google Scholar 

  3. Cordaux, R, Michel-Salzat, A, Bouchon, D (2001) Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol 14: 237–243

    Article  CAS  Google Scholar 

  4. Dobson, SL, Bourtzis, K, Braig, HR, Jones, BF, Zhou, WG, Rousset, F, O’Neill, SL (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 29: 153–160

    Article  PubMed  CAS  Google Scholar 

  5. Gray, SM, Banerjee, N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63: 128–148

    PubMed  CAS  Google Scholar 

  6. Heath, BD, Butcher, RDJ, Whitfield, WGF, Hubbard, SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9: 313–316

    Article  PubMed  CAS  Google Scholar 

  7. Holden, PR, Brookfield, JFY, Jones, P (1993) Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Mol Genet 240: 213–220

    Article  CAS  Google Scholar 

  8. Huigens, ME, de Almeida, RP, Boons, PAH, Luck, RF, Stouthamer, R (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc R Soc Lond B 271: 509–515

    Article  CAS  Google Scholar 

  9. Hurst, GDD, Hurst, LD, Majerus, MEN (1992) Selfish genes move sideways. Nature 356: 659–660

    Article  PubMed  CAS  Google Scholar 

  10. Jiggins, FM, Schulenburg, JHGvd, Hurst, GDD, Majerus, MEN (2001) Recombination confounds interpretations of Wolbachia evolution. Proc R Soc Lond B 268: 1423–1427

    Article  CAS  Google Scholar 

  11. Kittayapong, P, Jamnongluk, W, Thipaksorn, A, Milne, JR, Sindhusake, C (2003) Wolbachia infection complexity among insects in the tropical rice-field community. Mol Ecol 12: 1049–1060

    Article  PubMed  CAS  Google Scholar 

  12. Malloch, G, Fenton, B (2005) Super-infections of Wolbachia in byturid beetles and evidence for genetic transfer between A and B super-groups of Wolbachia. Mol Ecol 14: 627–637

    Article  PubMed  CAS  Google Scholar 

  13. Miles, PW (1968) Insect secretions in plants. AnnuRevPhytopathol 6: 137–164

    Article  CAS  Google Scholar 

  14. Mitsuhashi, W, Saiki, T, Wei, W, Kawakita, H, Sato, M (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Mol Biol 11: 577–584

    Article  PubMed  CAS  Google Scholar 

  15. Noda, H, Miyoshi, T, Zhang, Q, Watanabe, K, Deng, K, Hoshizaki, S (2001) Wolbachia infection shared among planthoppers (Homoptera : Delphacidae) and their endoparasite (Strepsiptera : Elenchidae): a probable case of interspecies transmission. Mol Ecol 10: 2101–2106

    Article  PubMed  CAS  Google Scholar 

  16. O’Neill, SL, Giordano, R, Colbert, AME, Karr, TL, Robertson, HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89: 2699–2702

    Article  PubMed  Google Scholar 

  17. Posada, D, Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818

    Article  PubMed  CAS  Google Scholar 

  18. Purcell, AH (1985) The ecology of bacterial and mycoplasma plant diseases spread by leafhoppers and planthoppers. In: Nault, LR, Rodriquez, JG (Eds.) The Leafhoppers and Planthoppers. Wiley, NY, pp 351–380

    Google Scholar 

  19. Rigaud, T, Juchault, P (1995) Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J Evol Biol 8: 249–255

    Article  Google Scholar 

  20. Sambrook, J, Fritsch, EF, Maniatis, T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  21. Sanger, F (1988) Sequences, sequences and sequences. Annu Rev Biochem 57: 1–28

    Article  PubMed  CAS  Google Scholar 

  22. Schilthuizen, M, Stouthamer, R (1997) Horizontal transmission of parthenogenesis-inducing microbes in Trichogramma wasps. Proc R Soc Lond B 264: 361–366

    Article  CAS  Google Scholar 

  23. Stevens, L, Giordano, R, Fialho, RF (2001) Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Ann Rev Ecol Syst 32: 519–545

    Article  Google Scholar 

  24. touthamer, R, Breeuwer, JAJ, Hurst, GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53: 71–102

    Article  PubMed  CAS  Google Scholar 

  25. Swofford, DL (1999) PAUP: Phylogenetic Analysis Using Parsimony. Centre for Agriculture and Bioscience International, Champaign, IL

    Google Scholar 

  26. Van Meer, MMM, Witteveldt, J, Stouthamer, R (1999) Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Mol Biol 8: 399–408

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  28. Werren, JH, Zhang, W, Guo, LR (1995) Evolution and phylogeny of Wolbachia-reproductive parasites of arthropods. Proc R Soc Lond B 261: 55–63

    Article  CAS  Google Scholar 

  29. Werren, JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587–609

    Article  PubMed  CAS  Google Scholar 

  30. Werren, JH, O’Neill, SL (1997) The evolution of heritable symbionts. In: O’Neill, SL, Hoffmann, AA, Werren, JH (Eds.) Influential Passengers. Inherited Microorganisms and Arthropod Reproduction. Oxford, New York, pp 1–42

    Google Scholar 

  31. Werren, JH, Bartos, JD (2001) Recombination in Wolbachia. Curr Biol 11: 431–435

    Article  PubMed  CAS  Google Scholar 

  32. Zhou, W, Rousset, F, O’Neill, SL (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B 265: 509–515

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Sanwapan Sanpittaya for cultivating pumpkin and loofah plants, Wanwisa Jamnongluk for phylogenetic analysis advice, Samnieng Theinthong and Nutchaya Klinpikul for technical assistance, Vichit Koonthong for insect and Sangvorn Kitthawee for parasitoid identification, Paul DeBarro for whitefly molecular identification, and Amporn Duangkaew for administrative support. This research was financed by the TRF/BIOTEC Special Program for Biodiversity Research and Training (BRT139026) and the Thailand Research Fund (RTA428001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. R. Milne.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sintupachee, S., Milne, J.R., Poonchaisri, S. et al. Closely Related Wolbachia Strains within the Pumpkin Arthropod Community and the Potential for Horizontal Transmission via the Plant. Microb Ecol 51, 294–301 (2006). https://doi.org/10.1007/s00248-006-9036-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9036-x

Keywords

Navigation