Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Sep 7;270(1526):1857–1865. doi: 10.1098/rspb.2003.2425

Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods.

Andrew R Weeks 1, Robert Velten 1, Richard Stouthamer 1
PMCID: PMC1691448  PMID: 12964989

Abstract

Many intracellular micro-organisms are now known to cause reproductive abnormalities and other phenomena in their hosts. The endosymbiont Wolbachia is the best known of these reproductive manipulators owing to its extremely high incidence among arthropods and the diverse host effects it has been implicated as causing. However, recent evidence suggests that another intracellular bacterium, a Cytophaga-like organism (CLO), may also induce several reproductive effects in its hosts. Here, we present the first survey of arthropod hosts for infection by the CLO. We use a sensitive hemi-nested polymerase chain reaction method to screen 223 species from 20 arthropod orders for infection by the CLO and Wolbachia. The results indicate that, although not as prevalent as Wolbachia, the CLO infects a significant number of arthropod hosts (ca. 7.2%). In addition, double infections of the CLO and Wolbachia were found in individuals of seven arthropod species. Sequencing analysis of the 16S rDNA region of the CLO indicates evidence for horizontal transmission of the CLO strains. We discuss these results with reference to future studies on host effects induced by intracellular micro-organisms.

Full Text

The Full Text of this article is available as a PDF (111.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Babcock C. S., Heraty J. M., De Barro P. J., Driver F., Schmidt S. Preliminary phylogeny of Encarsia Förster (Hymenoptera: Aphelinidae) based on morphology and 28S rDNA. Mol Phylogenet Evol. 2001 Feb;18(2):306–323. doi: 10.1006/mpev.2000.0875. [DOI] [PubMed] [Google Scholar]
  2. Bandi C., Dunn A. M., Hurst G. D., Rigaud T. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol. 2001 Feb;17(2):88–94. doi: 10.1016/s1471-4922(00)01812-2. [DOI] [PubMed] [Google Scholar]
  3. Clark J. W., Hossain S., Burnside C. A., Kambhampati S. Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective. Proc Biol Sci. 2001 Feb 22;268(1465):393–398. doi: 10.1098/rspb.2000.1390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Hoffmann A. A., Turelli M. Unidirectional incompatibility in Drosophila simulans: inheritance, geographic variation and fitness effects. Genetics. 1988 Jun;119(2):435–444. doi: 10.1093/genetics/119.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Huigens M. E., Luck R. F., Klaassen R. H., Maas M. F., Timmermans M. J., Stouthamer R. Infectious parthenogenesis. Nature. 2000 May 11;405(6783):178–179. doi: 10.1038/35012066. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hurst G. D., Jiggins F. M. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis. 2000 Jul-Aug;6(4):329–336. doi: 10.3201/eid0604.000402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jeyaprakash A., Hoy M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Kurtti T. J., Munderloh U. G., Andreadis T. G., Magnarelli L. A., Mather T. N. Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis. J Invertebr Pathol. 1996 May;67(3):318–321. doi: 10.1006/jipa.1996.0050. [DOI] [PubMed] [Google Scholar]
  12. Normark Benjamin B. The evolution of alternative genetic systems in insects. Annu Rev Entomol. 2002 Jun 4;48:397–423. doi: 10.1146/annurev.ento.48.091801.112703. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Posada D., Crandall K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. doi: 10.1093/bioinformatics/14.9.817. [DOI] [PubMed] [Google Scholar]
  15. Schilthuizen M., Stouthamer R. Horizontal transmission of parthenogenesis-inducing microbes in Trichogramma wasps. Proc Biol Sci. 1997 Mar 22;264(1380):361–366. doi: 10.1098/rspb.1997.0052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Stouthamer R., Breeuwert J. A., Luck R. F., Werren J. H. Molecular identification of microorganisms associated with parthenogenesis. Nature. 1993 Jan 7;361(6407):66–68. doi: 10.1038/361066a0. [DOI] [PubMed] [Google Scholar]
  18. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wade M. J., Stevens L. Microorganism mediated reproductive isolation in flour beetles (genus Tribolium). Science. 1985 Feb 1;227(4686):527–528. doi: 10.1126/science.3966160. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Werren J. H., Windsor D. M. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci. 2000 Jul 7;267(1450):1277–1285. doi: 10.1098/rspb.2000.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. West S. A., Cook J. M., Werren J. H., Godfray H. C. Wolbachia in two insect host-parasitoid communities. Mol Ecol. 1998 Nov;7(11):1457–1465. doi: 10.1046/j.1365-294x.1998.00467.x. [DOI] [PubMed] [Google Scholar]
  24. Yen J. H., Barr A. R. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature. 1971 Aug 27;232(5313):657–658. doi: 10.1038/232657a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES