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. 2003 Oct 22;270(1529):2185–2190. doi: 10.1098/rspb.2003.2475

A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella.

Martha S Hunter 1, Steve J Perlman 1, Suzanne E Kelly 1
PMCID: PMC1691482  PMID: 14561283

Abstract

Vertically transmitted symbionts of arthropods have been implicated in several reproductive manipulations of their hosts. These include cytoplasmic incompatibility (CI), parthenogenesis induction in haplodiploid species (PI), feminization and male killing. One symbiont lineage in the alpha-Proteobacteria, Wolbachia, is the only bacterium known to cause all of these effects, and has been thought to be unique in causing CI, in which the fecundity of uninfected females is reduced after mating with infected males. Here, we provide evidence that an undescribed symbiont in the Bacteroidetes group causes CI in a sexual population of the parasitic wasp Encarsia pergandiella. Wasps were crossed in all four possible combinations of infected and uninfected individuals. In the cross predicted to be incompatible, infected (I) males x uninfected (U) females, progeny production was severely reduced, with these females producing only 12.6% of the number of progeny in other crosses. The incompatibility observed in this haplodiploid species was the female mortality type; dissections showed that most progeny from the incompatible cross died as eggs. The 16S rDNA sequence of this symbiont is 99% identical to a parthenogenesis-inducing symbiont in other Encarsia, and 96% identical to a feminizing symbiont in haplodiploid Brevipalpus mites. Thus, this recently discovered symbiont lineage is capable of inducing three of the four principal manipulations of host reproduction known to be caused by Wolbachia.

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Selected References

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  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arakaki N., Miyoshi T., Noda H. Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proc Biol Sci. 2001 May 22;268(1471):1011–1016. doi: 10.1098/rspb.2001.1628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bandi C., Damiani G., Magrassi L., Grigolo A., Fani R., Sacchi L. Flavobacteria as intracellular symbionts in cockroaches. Proc Biol Sci. 1994 Jul 22;257(1348):43–48. doi: 10.1098/rspb.1994.0092. [DOI] [PubMed] [Google Scholar]
  4. Bandi C., Trees A. J., Brattig N. W. Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol. 2001 Jul 12;98(1-3):215–238. doi: 10.1016/s0304-4017(01)00432-0. [DOI] [PubMed] [Google Scholar]
  5. Bordenstein S. R., O'Hara F. P., Werren J. H. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature. 2001 Feb 8;409(6821):707–710. doi: 10.1038/35055543. [DOI] [PubMed] [Google Scholar]
  6. Breeuwer J. A., Werren J. H. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature. 1990 Aug 9;346(6284):558–560. doi: 10.1038/346558a0. [DOI] [PubMed] [Google Scholar]
  7. Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M. E., Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A. 2001 May 15;98(11):6247–6252. doi: 10.1073/pnas.101304298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gottlieb Yuval, Zchori-Fein Einat, Werren John H., Karr Timothy L. Diploidy restoration in Wolbachia-infected Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J Invertebr Pathol. 2002 Nov;81(3):166–174. doi: 10.1016/s0022-2011(02)00149-0. [DOI] [PubMed] [Google Scholar]
  9. Hinnebusch B. Joseph, Rosso Marie-Laure, Schwan Tom G., Carniel Elisabeth. High-frequency conjugative transfer of antibiotic resistance genes to Yersinia pestis in the flea midgut. Mol Microbiol. 2002 Oct;46(2):349–354. doi: 10.1046/j.1365-2958.2002.03159.x. [DOI] [PubMed] [Google Scholar]
  10. Horn M., Harzenetter M. D., Linner T., Schmid E. N., Müller K. D., Michel R., Wagner M. Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus'. Environ Microbiol. 2001 Jul;3(7):440–449. doi: 10.1046/j.1462-2920.2001.00210.x. [DOI] [PubMed] [Google Scholar]
  11. Hunter M. S., Woolley J. B. Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Annu Rev Entomol. 2001;46:251–290. doi: 10.1146/annurev.ento.46.1.251. [DOI] [PubMed] [Google Scholar]
  12. Hurst G. D., Bandi C., Sacchi L., Cochrane A. G., Bertrand D., Karaca I., Majerus M. E. Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited flavobacteria that kill males only. Parasitology. 1999 Feb;118(Pt 2):125–134. doi: 10.1017/s0031182098003655. [DOI] [PubMed] [Google Scholar]
  13. Jamnongluk Wanwisa, Kittayapong Pattamaporn, Baimai Visut, O'Neill Scott L. Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Curr Microbiol. 2002 Oct;45(4):255–260. doi: 10.1007/s00284-002-3746-1. [DOI] [PubMed] [Google Scholar]
  14. Jiggins F. M., Bentley J. K., Majerus M. E., Hurst G. D. How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling. Proc Biol Sci. 2001 Jun 7;268(1472):1123–1126. doi: 10.1098/rspb.2001.1632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Marchesi J. R., Sato T., Weightman A. J., Martin T. A., Fry J. C., Hiom S. J., Dymock D., Wade W. G. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol. 1998 Feb;64(2):795–799. doi: 10.1128/aem.64.2.795-799.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Masui S., Kamoda S., Sasaki T., Ishikawa H. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J Mol Evol. 2000 Nov;51(5):491–497. doi: 10.1007/s002390010112. [DOI] [PubMed] [Google Scholar]
  17. Moran Nancy A., Dale Colin, Dunbar Helen, Smith Wendy A., Ochman Howard. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ Microbiol. 2003 Feb;5(2):116–126. doi: 10.1046/j.1462-2920.2003.00391.x. [DOI] [PubMed] [Google Scholar]
  18. 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 U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. O'Sullivan Louise A., Weightman Andrew J., Fry John C. New degenerate Cytophaga-Flexibacter-Bacteroides-specific 16S ribosomal DNA-targeted oligonucleotide probes reveal high bacterial diversity in River Taff epilithon. Appl Environ Microbiol. 2002 Jan;68(1):201–210. doi: 10.1128/AEM.68.1.201-210.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ochman H., Lawrence J. G., Groisman E. A. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000 May 18;405(6784):299–304. doi: 10.1038/35012500. [DOI] [PubMed] [Google Scholar]
  21. Oliver Kerry M., Russell Jacob A., Moran Nancy A., Hunter Martha S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A. 2003 Jan 31;100(4):1803–1807. doi: 10.1073/pnas.0335320100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Poinsot Denis, Charlat Sylvain, Merçot Hervé. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. Bioessays. 2003 Mar;25(3):259–265. doi: 10.1002/bies.10234. [DOI] [PubMed] [Google Scholar]
  23. Sasaki Tetsuhiko, Kubo Takeo, Ishikawa Hajime. Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics. 2002 Nov;162(3):1313–1319. doi: 10.1093/genetics/162.3.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Somerson N. L., Ehrman L., Kocka J. P., Gottlieb F. J. Streptococcal L-forms isolated from Drosophila paulistorum semispecies cause sterility in male progeny. Proc Natl Acad Sci U S A. 1984 Jan;81(1):282–285. doi: 10.1073/pnas.81.1.282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
  26. Tram Uyen, Sullivan William. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science. 2002 May 10;296(5570):1124–1126. doi: 10.1126/science.1070536. [DOI] [PubMed] [Google Scholar]
  27. Van Meer M. M., Witteveldt J., Stouthamer R. Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Mol Biol. 1999 Aug;8(3):399–408. doi: 10.1046/j.1365-2583.1999.83129.x. [DOI] [PubMed] [Google Scholar]
  28. Vavre F., Fleury F., Varaldi J., Fouillet P., Boulétreau M. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution. 2000 Feb;54(1):191–200. doi: 10.1111/j.0014-3820.2000.tb00019.x. [DOI] [PubMed] [Google Scholar]
  29. Weeks A. R., Marec F., Breeuwer J. A. A mite species that consists entirely of haploid females. Science. 2001 Jun 29;292(5526):2479–2482. doi: 10.1126/science.1060411. [DOI] [PubMed] [Google Scholar]
  30. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991 Jan;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Werren J. H., Bartos J. D. Recombination in Wolbachia. Curr Biol. 2001 Mar 20;11(6):431–435. doi: 10.1016/s0960-9822(01)00101-4. [DOI] [PubMed] [Google Scholar]
  32. Werren J. H. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. doi: 10.1146/annurev.ento.42.1.587. [DOI] [PubMed] [Google Scholar]
  33. Werren J. H., Zhang W., Guo L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci. 1995 Jul 22;261(1360):55–63. doi: 10.1098/rspb.1995.0117. [DOI] [PubMed] [Google Scholar]

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