1887

Abstract

Previously, analysis of 16S rDNA sequences placed a newly discovered lineage of bacterial symbionts of arthropods in the ‘’. This symbiont lineage is associated with a number of diverse host reproductive manipulations, including induction of parthenogenesis in several parasitoid wasps (Hymenoptera: Aphelinidae). In this study, electron microscopy and phylogenetic analysis of the 16S rRNA and genes of symbionts from and are used to describe and further characterize these bacteria. Phylogenetic analyses based on these two genes showed that the symbionts are allied with the lineage within the ‘’, with their closest described relative being the acanthamoeba symbiont ‘ Amoebophilus asiaticus’. The symbionts share 97 % 16S rDNA sequence similarity with mite and tick symbionts and 88 % sequence similarity with ‘ A. asiaticus’. Electron microscopy revealed that many of the bacteria found in the ovaries of the two species contained a regular, brush-like array of microfilament-like structures that appear to be characteristic of the symbiont. Finally, the role of this bacterium in parthenogenesis induction in was confirmed. Based on phylogenetic analyses and electron microscopy, classification of the symbionts from as ‘ Cardinium hertigii’ is proposed.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.02957-0
2004-05-01
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/54/3/ijs540961.html?itemId=/content/journal/ijsem/10.1099/ijs.0.02957-0&mimeType=html&fmt=ahah

References

  1. Aksoy S. 2000; Tsetse – a haven for microorganisms. Parasitol Today 16:114–118 [CrossRef]
    [Google Scholar]
  2. Buchner P. 1965 Endosymbiosis of Animals with Plant Microorganisms New York: Wiley;
    [Google Scholar]
  3. Bull J. J. 1983 Evolution of Sex Determining Mechanisms Menlo Park, CA: Benjamin–Cummings;
    [Google Scholar]
  4. Chang K. P., Musgrave A. J. 1972; Multiple symbiosis in a leafhopper, Helochara communis Fitch (Cicadellidae: Homoptera): envelopes, nucleoids and inclusions of the symbiotes. J Cell Sci 11:275–293
    [Google Scholar]
  5. Cole J. R., Chai B., Marsh T. L. 8 other authors 2003; The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443 [CrossRef]
    [Google Scholar]
  6. Costa H. S., Westcot D. M., Ullman D. E., Rosell R., Brown J. K., Johnson M. W. 1995; Morphological variation in Bemisia endosymbionts. Protoplasma 189:194–202 [CrossRef]
    [Google Scholar]
  7. Dolan M. F. 2001; Speciation of termite gut protists: the role of bacterial symbionts. Int Microbiol 4:203–208 [CrossRef]
    [Google Scholar]
  8. Douglas A. E. 1998; Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera . Annu Rev Entomol 43:17–37 [CrossRef]
    [Google Scholar]
  9. Endo B. Y. 1979; The ultrastructure and distribution of an intracellular bacterium-like microorganism in tissues of larvae of the soybean cyst nematode, Heterodera glycines . J Ultrastruct Res 67:1–14 [CrossRef]
    [Google Scholar]
  10. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [CrossRef]
    [Google Scholar]
  11. Garrity G. M., Holt J. G. 2001; The road map to the Manual . In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp  119–166 Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
    [Google Scholar]
  12. Giorgini M. 2001; Induction of males in thelytokous populations of Encarsia meritoria and Encarsia protransvena : a systematic tool. Biocontrol 46:427–438 [CrossRef]
    [Google Scholar]
  13. Grenier A. M., Nardon C., Nardon P. 1994; The role of symbiotes in flight activity of Sitophilus weevils. Entomol Exp Appl 70:201–208 [CrossRef]
    [Google Scholar]
  14. Hertig M. 1936; The rickettsia, Wolbachia pipientis (gen. et sp. n.) and associated inclusions of the mosquito, Culex pipiens . Parasitology 28:453–486 [CrossRef]
    [Google Scholar]
  15. Hess R. T., Hoy M. A. 1982; Microorganisms associated with the spider mite predator Metaseiulus (= Typhlodromus ) occidentalis : electron microscope observations. J Invertebr Pathol 40:98–106 [CrossRef]
    [Google Scholar]
  16. Horn M., Harzenetter M. D., Linner T., Schmid E. N., Müller K.-D., Michel R., Wagner M. 2001; Members of the Cytophaga - Flavobacterium - Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of ‘ Candidatus Amoebophilus asiaticus’. Environ Microbiol 3:440–449 [CrossRef]
    [Google Scholar]
  17. Huang W. M. 1996; Bacterial diversity based on type II DNA topoisomerase genes. Annu Rev Genet 30:79–107 [CrossRef]
    [Google Scholar]
  18. Hunter M. S. 1999; The influence of parthenogenesis-inducing Wolbachia on the oviposition behavior and sex-specific developmental requirements of autoparasitoid wasps. J Evol Biol 12:735–741 [CrossRef]
    [Google Scholar]
  19. Hunter M. S., Perlman S. J., Kelly S. E. 2003; A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella . Proc R Soc Lond B Biol Sci 270:2185–2190 [CrossRef]
    [Google Scholar]
  20. Kurtti T. J., Munderloh U. G., Andreadis T. G., Magnarelli L. A., Mather T. N. 1996; Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis . J Invertebr Pathol 67:318–321 [CrossRef]
    [Google Scholar]
  21. Ludwig W., Strunk O., Klugbauer S., Klugbauer N., Weizenegger M., Neumaier J., Bachleitner M., Schleifer K.-H. 1998; Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568 [CrossRef]
    [Google Scholar]
  22. Maddison D. R., Maddison W. P. 2001 MacClade version 4.0.1 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  23. Montllor C. B., Maxmen A., Purcell A. H. 2002; Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195 [CrossRef]
    [Google Scholar]
  24. Moran N. A., Telang A. 1998; Bacteriocyte-associated symbionts of insects. Bioscience 48:295–304 [CrossRef]
    [Google Scholar]
  25. Moran N. A., Dale C., Dunbar H., Smith W. A., Ochman H. 2003; Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ Microbiol 5:116–126 [CrossRef]
    [Google Scholar]
  26. Murray R. G. E., Stackebrandt E. 1995; Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187 [CrossRef]
    [Google Scholar]
  27. Oliver K. M., Russell J. A., Moran N. A., Hunter M. S. 2003; Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807 [CrossRef]
    [Google Scholar]
  28. Polaszek A., Evans G. A., Bennett F. D. 1992; Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification. Bull Entomol Res 82:375–392 [CrossRef]
    [Google Scholar]
  29. Stackebrandt E., Goebel B. M. 1994; Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849 [CrossRef]
    [Google Scholar]
  30. Stouthamer R., Breeuwer J. A. J., Hurst G. D. D. 1999; Wolbachia pipientis : microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102 [CrossRef]
    [Google Scholar]
  31. Swofford D. L. 2001 paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  32. 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 [CrossRef]
    [Google Scholar]
  33. Weeks A. R., Breeuwer J. A. J. 2003; A new bacterium from the Cytophaga - Flavobacterium - Bacteroides phylum that causes sex-ratio distortion. In Insect Symbiosis pp  165–176 Edited by Bourtzis K., Miller T. A. New York: CRC Press;
    [Google Scholar]
  34. Weeks A. R., Marec F., Breeuwer J. A. J. 2001; A mite species that consists entirely of haploid females. Science 292:2479–2482 [CrossRef]
    [Google Scholar]
  35. Weeks A. R., Velten R., Stouthamer R. 2003; Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B Biol Sci 270:1857–1865 [CrossRef]
    [Google Scholar]
  36. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
    [Google Scholar]
  37. Yamamoto S., Harayama S. 1995; PCR amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol 61:1104–1109
    [Google Scholar]
  38. Zchori-Fein E., Gottlieb Y., Kelly S. E., Brown J. K., Wilson J. M., Karr T. L., Hunter M. S. 2001; A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci U S A 98:12555–12560 [CrossRef]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijs.0.02957-0
Loading
/content/journal/ijsem/10.1099/ijs.0.02957-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error