Current Microbiology

, Volume 65, Issue 5, pp 516–523 | Cite as

Wolbachia Strengthens Cardinium-Induced Cytoplasmic Incompatibility in the Spider Mite Tetranychus piercei McGregor

  • Lu-Yu Zhu
  • Kai-Jun Zhang
  • Yan-Kai Zhang
  • Cheng Ge
  • Tetsuo Gotoh
  • Xiao-Yue HongEmail author


Wolbachia and Cardinium are maternally inherited intracellular bacteria that can manipulate the reproduction of their arthropod hosts, such as by inducing cytoplasmic incompatibility (CI). Although the reproductive alteration induced by Wolbachia or Cardinium have been well investigated, the effects of these two endosymbionts co-infecting the same host are poorly understood. We found that Tetranychus piercei McGregor is naturally infected with Wolbachia and Cardinium. We performed all possible crossing combinations using naturally infected and cured strains, and the results show that Wolbachia induced a weak level of CI, while Cardinium-infected and doubly infected males caused severe CI. Wolbachia and Cardinium could not rescue CI each other; however, Wolbachia boosted the expression of Cardinium-induced CI. Quantitative PCR results demonstrated that CI was associated with the infection density of Wolbachia and Cardinium.


Bacterial Density Infected Male Cytoplasmic Incompatibility Isofemale Line Wolbachia Strain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Baldo L, Dunning Hotopp JC, Jolley KA et al (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72:7098–7110PubMedCrossRefGoogle Scholar
  2. 2.
    Barr AR (1980) Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature 283:71–72PubMedCrossRefGoogle Scholar
  3. 3.
    Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ (2006) The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Pathog 2:e43PubMedCrossRefGoogle Scholar
  4. 4.
    Bourtzis K, Dobson SL, Braig HR, O’Neill SL (1998) Rescuing Wolbachia have been overlooked. Nature 391:852–853PubMedCrossRefGoogle Scholar
  5. 5.
    Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144:1063–1073PubMedGoogle Scholar
  6. 6.
    Braig HR, Zhou W, Dobson SL, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180:2373–2378PubMedGoogle Scholar
  7. 7.
    Breeuwer JAJ (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41–47CrossRefGoogle Scholar
  8. 8.
    Breeuwer JAJ, Werren JH (1993) Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135:565–574PubMedGoogle Scholar
  9. 9.
    Callaini G, Riparbelli MG, Giordano R, Dallai R (1996) Mitotic defects associated with cytoplasmic incompatibility in Drosophila simulans. J Invertebr Pathol 67:55–64CrossRefGoogle Scholar
  10. 10.
    Dobson SL, Marsland EJ, Rattanadechakul W (2001) Wolbachia-induced cytoplasmic incompatibility in single-and super-infected Aedes albopictus (Diptera: Culicidae). J Med Entomol 38:382–387PubMedCrossRefGoogle Scholar
  11. 11.
    Duron O, Hurst GDD, Hornett EA, Josling JA, Engelstädter J (2008) High incidence of the maternally inherited bacterium Cardinium in spiders. Mol Ecol 17:1427–1437PubMedCrossRefGoogle Scholar
  12. 12.
    Gotoh T, Noda H, Ito S (2006) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13–20PubMedCrossRefGoogle Scholar
  13. 13.
    Gottlieb Y, Ghanim M, Gueguen G et al (2008) Inherited intracellular ecosystem: symbiotic bacteria share the bacteriocytes of whiteflies. FASEB J 22:2591–2599PubMedCrossRefGoogle Scholar
  14. 14.
    Groot TVM, Breeuwer JAJ (2006) Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Exp Appl Acarol 39:257–271PubMedCrossRefGoogle Scholar
  15. 15.
    Hoffmann A, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, Oxford, pp 42–80Google Scholar
  16. 16.
    Hunter MS, Perlman SJ, Kelly SE (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc R Soc Lond B 270:2185–2190CrossRefGoogle Scholar
  17. 17.
    Kondo N, Shimada M, Fukatsu T (2005) Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 1:488–491PubMedCrossRefGoogle Scholar
  18. 18.
    Morimoto S, Kurtti TJ, Noda H (2006) In vitro cultivation and antibiotic susceptibility of a Cytophaga-like intracellular symbiote isolated from the tick Ixodes scapularis. Curr Microbiol 52:324–329PubMedCrossRefGoogle Scholar
  19. 19.
    Mouton L, Henri H, Bouletreau M, Vavre F (2003) Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol Ecol 12:3459–3465PubMedCrossRefGoogle Scholar
  20. 20.
    Mouton L, Henri H, Bouletreau M, Vavre F (2005) Multiple infections and diversity of cytoplasmic incompatibility in a haplodiploid species. Heredity 94:187–192PubMedCrossRefGoogle Scholar
  21. 21.
    Noda H, Koizumi Y, Zhang Q, Deng K (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem Mol Biol 31:727–737PubMedCrossRefGoogle Scholar
  22. 22.
    Reynolds KT, Hoffmann AA (2002) Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet Res 80:79–87PubMedCrossRefGoogle Scholar
  23. 23.
    Ros VID, Breeuwer JAJ (2007) Spider mite (Acari: Tetranychidae) mitochondrial COI phylogeny reviewed: host plant relationships, phylogeography, reproductive parasites and barcoding. Exp Appl Acarol 42:239–262PubMedCrossRefGoogle Scholar
  24. 24.
    Ros VID, Breeuwer JAJ (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102:413–422PubMedCrossRefGoogle Scholar
  25. 25.
    Sinkins SP, Braig HR, O’Neill SL (1995) Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Exp Parasitol 81:284–291PubMedCrossRefGoogle Scholar
  26. 26.
    Stouthamer R, Breeuwer J, Hurst G (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102PubMedCrossRefGoogle Scholar
  27. 27.
    Tram U, Ferree PM, Sullivan W (2003) Identification of Wolbachia-host interacting factors through cytological analysis. Microbes Infect 5:999–1011PubMedCrossRefGoogle Scholar
  28. 28.
    Van Opijnen T, Breeuwer JAJ (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23:871–881PubMedCrossRefGoogle Scholar
  29. 29.
    Vautrin E, Charles S, Genieys S, Vavre F (2007) Evolution and invasion dynamics of multiple infections with Wolbachia investigated using matrix based models. J Theor Biol 245:197–209PubMedCrossRefGoogle Scholar
  30. 30.
    Vavre F, Fleury F, Varaldi J, Fouillet P, Boulétreau M (2000) Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution 54:191–200PubMedGoogle Scholar
  31. 31.
    Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K (2004) Heads or tails: host-parasite interactions in the DrosophilaWolbachia system. Appl Environ Microbiol 70:5366–5372PubMedCrossRefGoogle Scholar
  32. 32.
    Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, Bourtzis K (2003) Cytoplasmic incompatibility and sperm cyst infection in different DrosophilaWolbachia associations. Genetics 164:545–552PubMedGoogle Scholar
  33. 33.
    Watanabe M, Miura K, Hunter M, Wajnberg E (2011) Superinfection of cytoplasmic incompatibility-inducing Wolbachia is not additive in Orius strigicollis (Hemiptera: Anthocoridae). Heredity 106:642–648PubMedCrossRefGoogle Scholar
  34. 34.
    Weeks AR, Tracy Reynolds K, Hoffmann AA (2002) Wolbachia dynamics and host effects: what has (and has not) been demonstrated? Trends Ecol Evol 17:257–262CrossRefGoogle Scholar
  35. 35.
    Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270:1857–1865CrossRefGoogle Scholar
  36. 36.
    Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609PubMedCrossRefGoogle Scholar
  37. 37.
    Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751PubMedCrossRefGoogle Scholar
  38. 38.
    Werren JH, O’Neill SL (1997) Inherited microorganisms and arthropod reproduction. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, Oxford, pp 1–41Google Scholar
  39. 39.
    Werren JH, Windsor D, Guo L (1995) Distribution of Wolbachia among neotropical arthropods. Proc R Soc Lond B 262:197–204CrossRefGoogle Scholar
  40. 40.
    White JA, Kelly SE, Perlman SJ, Hunter MS (2009) Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron: disentangling the roles of Cardinium and Wolbachia symbionts. Heredity 102:483–489PubMedCrossRefGoogle Scholar
  41. 41.
    Xie RR, Chen XL, Hong XY (2011) Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Appl Entomol Zool 46:95–102CrossRefGoogle Scholar
  42. 42.
    Xie RR, Zhou LL, Zhao ZJ, Hong XY (2010) Male age influences the strength of Cardinium-induced cytoplasmic incompatibility expression in the carmine spider mite Tetranychus cinnabarinus. Appl Entomol Zool 45:417–423CrossRefGoogle Scholar
  43. 43.
    Zabalou S, Apostolaki A, Pattas S, Veneti Z, Paraskevopoulos C, Livadaras I et al (2008) Multiple rescue factors within a Wolbachia strain. Genetics 178:2145–2160PubMedCrossRefGoogle Scholar
  44. 44.
    Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Lu-Yu Zhu
    • 1
  • Kai-Jun Zhang
    • 1
  • Yan-Kai Zhang
    • 1
  • Cheng Ge
    • 1
  • Tetsuo Gotoh
    • 2
  • Xiao-Yue Hong
    • 1
    Email author
  1. 1.Department of EntomologyNanjing Agricultural UniversityNanjingChina
  2. 2.Laboratory of Applied Entomology and Zoology, Faculty of AgricultureIbaraki UniversityAmiJapan

Personalised recommendations