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Molecular evidence for the endosymbiont Wolbachia in a non-filaroid nematode, Angiostrongylus cantonensis

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Journal of Biomedical Science

Summary

Wolbachia harbored by most filarial parasites, is critical to both embryogenesis and microfilarial development, and may lead to inflammation and pathogenesis in infected hosts. Based on alignment of the sequences from the wsp, ftsZ, and 16S rRNA genes, Wolbachia was demonstrated to exist in Angiostrongylus cantonensis, a non-filaroid nematode. Although the wsp gene may not be the best candidate for evolutionary analysis of Wolbachia, this gene has been sequenced from a broader coverage of the host species, making it feasible to be used for phylogenetic analysis in this study. The results from both Neighbor-joining and Maximum parsimony methods showed that this novel Wolbachia does not belong to any of the known groups (C or D) of nematode-derived Wolbachia. In addition, the wsp gene sequence of this newly identified endosymbiont revealed a high degree of identity (98%) with that from Diaea circumlita c2, tentatively classified into the putative group G. This suggests that Wolbachia from A. cantonensis could represent a deeply branched lineage in Wolbachia evolution or the occurrence of horizontal transfer between infected hosts. In conclusion, the findings provide some insights into our understanding of the evolution of Wolbachia, particularly the isolate from A. cantonensis.

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References

  1. O’Neill S.L., Pettigrew M.M., Sinkins S.P., Braig H.R., Andreadis T.G., Tesh R.B. (1997) In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol. Biol. 6:33–39

    Article  PubMed  CAS  Google Scholar 

  2. Werren J.H. (1997) Biology of Wolbachia. Annu. Rev. Entomol. 42:587–609

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  4. Bazzocchi C., Jamnongluk W., O’Neill S.L., Anderson T.J.C., Genchi C., Bandi C. (2000) wsp gene sequences from the Wolbachia of filarial nematodes. Curr. Microbiol. 41:96–100

    Article  PubMed  CAS  Google Scholar 

  5. Anderson C.L., and Karr T.L., Wolbachia: evolutionary novelty in a rickettsial bacteria. BMC Evo. Biol. 1:http://www.biomedcentral.com/1471-2148/1/10, 2001

  6. Sironi M., Bandi C., Sacchi L., Di Sacco B., Damiani G., Genchi C. (1995) Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol. Biochem. Parasitol. 74:223–227

    Article  PubMed  CAS  Google Scholar 

  7. Taylor M.J., Bilo K., Cross H.F., Archer J.P. and Underwood A.P., (1999) 16S rDNA phylogeny and ultrastructural characterization of Wolbachia intracellular bacteria of the filarial nematodes Brugia malayi, B. pahangi, and Wuchereria bancrofti. Exp. Parasitol. 91:356–361

    Article  PubMed  CAS  Google Scholar 

  8. Büttner D.W., Wanji S., Bazzocchi C., Bain O., and Fischer␣P., Obligatory symbiotic Wolbachia endobacteria are absent from Loa loa. Filaria J. 2:http://www.filariajournal.com/content/2/1/10, 2003

  9. McGarry H.F., Pfarr K., Egerton G., Hoerauf A., Akue J., Enyong P., Wanji S., Klager S.L., Bianco A.E., Beeching N.J. and Taylor M.J., Evidence against Wolbachia symbiosis in Loa loa. Filaria J. 2:http://www.filariajournal.com/content/2/1/9, 2003

  10. Hise A.G., Gillette-Ferguson I., Pearlman E. (2004) The role of endosymbiotic Wolbachia bacteria in filarial disease. Cell. Microbiol. 6:97–104

    Article  PubMed  CAS  Google Scholar 

  11. Peixoto C.A., Silva L.F., Teixeira K.M., Rocha A. (2001) Ultrastructural characterization of intracellular bacteria of Wuchereria bancrofti. Trans. R. Soc. Trop. Med. Hyg. 95:566–568

    Article  PubMed  CAS  Google Scholar 

  12. Brattig N.W. (2004) Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes Infect. 6:113–128

    Article  PubMed  CAS  Google Scholar 

  13. McGarry H.F., Egerton G.L., Taylor M.J. (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol. Biochem. Parasitol. 135:57–67

    Article  PubMed  CAS  Google Scholar 

  14. Taylor M.J., Bandi C., Hoerauf A., Lazdins J. (2000) Wolbachia bacteria of filarial nematodes: a target for control? Parasitol. Today 16:179–180

    Article  PubMed  CAS  Google Scholar 

  15. Brattig N.W., Büttner D.W., Hoerauf A. (2001) Neutrophil accumulation around Onchocerca worms and chemotaxis of neutrophils are dependent on Wolbachia endobacteria. Microbes Infect. 3:439–446

    Article  PubMed  CAS  Google Scholar 

  16. André A.v.S., Blackwell N.M., Hall L.R., Hoerauf A., Brattig N.W., Volkmann L., Taylor M.J., Ford L., Hise A.G., Lass J.H., Diaconu E., Pearlman E. (2002) The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science 295:1892–1895

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Tsai H.C., Liu Y.C., Kunin C.M., Lee S.S., Chen Y.S., Lin H.H., Tsai T.H., Lin W.R., Huang C.K., Yen M.Y., Yen C.M. (2001) Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. Am. J. Med. 111:109–114

    Article  PubMed  CAS  Google Scholar 

  19. Wang L.C., Wan Y.L. (2004) Alteration of antibodies against the fifth-stage larvae and changes in brain magnetic resonance images in experimentally infected rabbits with Angiostrongylus cantonensis. J. Parasitol. 90:1193–1196

    Article  PubMed  Google Scholar 

  20. Casiraghi M., Favia G., Cancrini G., Bartoloni A., Bandi C. (2001) Molecular identification of Wolbachia from the filarial nematode Mansonella ozzardi. Parasitol. Res. 87:417–420

    Article  PubMed  CAS  Google Scholar 

  21. Tsai K.H., Lien J.C., Huang C.G., Wu W.J., Chen W.J. (2004) Molecular (sub-)grouping of the endosymbiont Wolbachia infection among mosquitoes of Taiwan. J. Med. Entomol. 41:677–683

    Article  PubMed  CAS  Google Scholar 

  22. Thompson J.D., Higgins D.G., Gibson T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  23. Kumar S., Tamura K., Jakobsen I.B., Nei M. (2001) MEGA2: Molecular evolutionary genetics analysis software. Arizona State University, Tempe, AZ, USA

    Google Scholar 

  24. Lo N., Casiraghi M, Salati E, Bazzocchi C, Bandi C. (2002) How many Wolbachia supergroups exist? Mol. Biol. Evol. 19:341–346

    PubMed  CAS  Google Scholar 

  25. Tsai K.H., Phylogeny of the symbiont Wolbachia in mosquitoes and its potential interactions with arbovirus in the mosquito. PhD dissertation, National Taiwan University, Taipei, Taiwan, 2004, pp.117

  26. Taylor M.J., Hoerauf A. (1999) Wolbachia bacteria of filarial nematodes. Parasitol. Today 5:437–442

    Article  PubMed  CAS  Google Scholar 

  27. Bordenstein S.R., Fitch D.H., Werren J.H. (2003) Absence of Wolbachia in nonfilariid nematodes. J. Nematol. 35:266–270

    PubMed  Google Scholar 

  28. Blaxter M.L., de Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J.R., Mackey L.Y., Dorris M., Frisse L.M., Vida J.T., Thomas W.K. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

    Article  PubMed  CAS  Google Scholar 

  29. Bandi C., Anderson T.J.C., Genchi C., Blaxter M.L. (1998) Phylogeny of Wolbachia in filarial nematodes. Proc. R. Soc. Lond. Ser. B 265:2407–2413

    Article  CAS  Google Scholar 

  30. Casiraghi M., Bain O., Guerrero R., Martin C., Pocacqua V., Gardner S.L., Franceschi A., Bandi C. (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Intl. J. Parasitol. 34:191–203

    Article  Google Scholar 

  31. Hong X.Y., Gotoh T., Noda H. (2002) Sensitivity comparison of PCR primers for detecting Wolbachia in spider mites. Appl. Entomol. Zool. 37:379–383

    Article  CAS  Google Scholar 

  32. Egyed Z., Sréter T., Széll Z., Nyirő G., Dobos-Kovács M., Márialigeti K., Varga I. (2004) Electron microscopic and molecular identification of Wolbachia endosymbionts from Onchocerca lupi: implications for therapy. Vet. Parasitol. 106:75–82

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  34. Werren J.H., Zhang W., Guo L.R. (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lon. Ser. B 261:55–63

    Article  CAS  Google Scholar 

  35. Casiraghi M., Anderson T.J., Bandi C., Bazzocchi C., Genchi C. (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122:93–103

    Article  PubMed  CAS  Google Scholar 

  36. Vandekerckhove T.T.M., Watteyne S., Willems A., Swings J.G., Mertens J., Gillis M. (1999) Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy. FEMS Microbiol. Lett. 180:279–286

    PubMed  CAS  Google Scholar 

  37. Bandi C., Trees A.J., Brattig N.W. (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet. Parasitol. 98:215–238

    Article  PubMed  CAS  Google Scholar 

  38. Rowley S.M., Raven R.J., McGraw E.A. (2004) Wolbachia pipiens in Australian spiders. Curr. Microbiol. 49:208–214

    Article  PubMed  CAS  Google Scholar 

  39. Punkosdy G.A., Dennis V.A., Lasater B.L., Tzertzinis G., Foster J.M., Lammie P.J. (2001) Detection of serum IgG antibodies specific for Wolbachia surface protein in rhesus monkeys infected with Brugia malayi. J. Infect. Dis. 184:385–389

    Article  PubMed  CAS  Google Scholar 

  40. Kanpittaya J., Jitpimolmard S., Tiamka S., Mairiang E. (2000) MR findings of eosinophilic meningoencephalitis attributed to Angiostrongylus cantonensis. Am. J. Neuroradiol. 21:1090–1094

    PubMed  CAS  Google Scholar 

  41. Pien F.D., Pien B.C. (1999) Angiostrongylus cantonensis eosinophilic meningitis. Intl. J. Infect. Dis. 3:161–163

    Article  CAS  Google Scholar 

  42. Aoki M., Sugaya H., Ishida K., Yoshimura K. (1998) The role of CD4+ and CD8+ T-cells in host morbidity and innate resistance to Angiostrongylus cantonensis in the mouse. Parasitol. Res. 84:91–99

    Article  PubMed  CAS  Google Scholar 

  43. Taylor M.J. (2000) Wolbachia bacteria of filarial nematodes in the pathogenesis of disease and as a target for control. Trans. R. Soc. Trop. Med. Hyg. 94:596–598

    Article  PubMed  CAS  Google Scholar 

  44. Alto W. (2001) Human infections with Angiostrongylus cantonensis. Pac. Hlth. Dialog. 8:176–182

    CAS  Google Scholar 

  45. Mohanty B.P. (2001) Wolbachia: potential targets for control of filariases. Curr. Sci. 80:614–616

    Google Scholar 

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Acknowledgments

This work was financially supported by a grant from the National Science Council of Taiwan (NSC95-2320-B-182-017) and partially supported by Chang Gung Memorial Hospital (CMRP 150251).

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Correspondence to Wei-June Chen.

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Kun-Hsien Tsai and Chin-Gi Huang are contributed equally to this study

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Tsai, KH., Huang, CG., Wang, LC. et al. Molecular evidence for the endosymbiont Wolbachia in a non-filaroid nematode, Angiostrongylus cantonensis . J Biomed Sci 14, 607–615 (2007). https://doi.org/10.1007/s11373-007-9181-3

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  • DOI: https://doi.org/10.1007/s11373-007-9181-3

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