SpringerLink
Log in

Biological effects of the symbiosis between insects and intracellular bacteria Wolbachia pipientis

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Only a few decades ago, symbiosis between insects and bacteria was considered a relatively rare phenomenon. The concept of symbiosis has changed in the past two decades due to the development of molecular-genetic methods. At the same time, a peculiar variant of symbiotic relationships, reproductive parasitism (i.e., modification of the host reproductive strategy by symbiotic bacteria) has been actively discussed by researchers. The intracytoplasmic bacterium Wolbachia pipientis is the most common reproductive symbiont of insects. The age of the symbiosis between the Wolbachia and insects is estimated to be 150 million years. The biological effects of the bacterium on different insect species vary from sporadic asymptomatic carriage to obligate symbiosis with many intermediate forms. Each of the millions of insect species infected with Wolbachia develops its own unique genetic mechanisms of the interaction with the bacterium. New events of infection of insect species with Wolbachia and its losses occur quite often, and not only in evolutionary time periods. The present review summarizes the current data on the genetic control of modification of the insect reproductive behavior caused by the Wolbachia and data on the effect of Wolbachia on the adaptation of infected insects. The paper also presents the data on the relatively poorly studied process of genetic recombination in representatives of the bacterial genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akman, L., Yamashita, A., Watanabe, H., et al., Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia, Nat. Genet., 2002, vol. 32, pp. 402–407.

    Article  CAS  PubMed  Google Scholar 

  • Alexandrov, I.D., Alexandrova, M.V., Goryacheva, I.I., Shaikevich, E.V., Zakharov, I.A., and Rochina, N.V., Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster, Russ. J. Genet., 2007, vol. 43, no. 10, pp. 1147–1152.

    Article  CAS  Google Scholar 

  • Arakaki, N., Miyoshi, T., and Noda, H., Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta), Proc. R. Soc. Lond. B, 2001, vol. 268, no. 1471, pp. 1011–1016.

    Article  CAS  Google Scholar 

  • Asgharian, H., Chang, L., Mazzoglio, P.J., and Negri, I., Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner, Front. Microbiol., 2014, vol. 5, art. ID 430.

  • Ashburner, M., Drosophila, A Laboratory Handbook, New York: Cold Spring Harbor Lab. Press, 1989.

    Google Scholar 

  • Baldo, L., Bordenstein, S., Wernegreen, J.J., and Werren, J.H., Widespread recombination throughout Wolbachia genomes, Mol. Biol. Evol., 2006, vol. 23, no. 2, pp. 437–449.

    Article  CAS  PubMed  Google Scholar 

  • Bian, G., Joshi, D., Dong, Y., et al., Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection, Science, 2013, vol. 340, pp. 748–751.

    Article  CAS  PubMed  Google Scholar 

  • Bian, G., Xu, Y., Lu, P., et al., The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti, PLoS Pathog., 2010, vol. 6, p. e1000833.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bordenstein, S.R., Uy, J.J., and Werren, J.H., Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia, Genetics, 2003, vol. 164, pp. 223–233.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bourtzis, K., Nigrianaki, A., Markakis, G., and Savakis, C., Wolbachia infection and cytoplasmic incompatibility in Drosophila species, Genetics, 1996, vol. 144, pp. 1063–1073.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breeuwer, J.A. and Werren, J.H., Microorganisms associated with chromosome destruction and reproductive isolation between insect species, Nature, 1990, vol. 346, pp. 558–560.

    Article  CAS  PubMed  Google Scholar 

  • Brendza, R.P., Serbus, L.R., Duffy, J.B., and Saxton, W.M., A function for kinesin I in the posterior transport of Oskar mRNA and Staufen protein, Science, 2000, vol. 289, pp. 2120–2122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brendza, R.P., Serbus, L.R., Saxton, W.M., and Duffy, J.B., Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes, Curr. Biol., 2002, vol. 12, pp. 1541–1545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brownlie, J.C., Cass, B.N., Riegler, M., et al., Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress, PLoS Pathog., 2009, vol. 5, no. 4, p. e1000368.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Callaini, G., Dallai, R., and Riparbelli, M.G., Wolbachiainduced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans, J. Cell Sci., 1997, vol. 110, part 2, pp. 271–280.

    CAS  PubMed  Google Scholar 

  • Callaini, G., Riparbelli, M.G., and Dallai, R., The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules, J. Cell Sci., 1994, vol. 107, part 3, pp. 673–682.

    PubMed  Google Scholar 

  • Calvitti, M., Moretti, R., Lampazzi, E., et al., Characterization of a new Aedes albopictus (Diptera: Culicidae)—Wolbachia pipientis (Rickettsiales: Rickettsiaceae) symbiotic association generated by artificial transfer of the wPip strain from Culex pipiens (Diptera: Culicidae), J. Med. Entomol., 2010, vol. 47, no. 2, pp. 179–187.

    PubMed  Google Scholar 

  • Caragata, E.P., Rancè, E., Lauren, M., et al., Dietary cholesterol modulates pathogen blocking by Wolbachia, PLoS Pathog., 2013, vol. 9, no. 6, p. e1003459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho, K.-O., Kim, G.-W., and Lee, O.-K., Wolbachia bacteria reside in host golgi-related vesicles whose position is regulated by polarity proteins, PLoS One, 2011, no. 6, p. e22703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chrostek, E., Marialva, M.S.P., Esteves, S.S., et al., Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis, PLoS Genet., 2013, vol. 9, no. 12, p. e1003896.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chrostek, E. and Teixeira, L., Mutualism breakdown by amplification of Wolbachia genes, PLoS Biol., 2015, vol. 13, no. 2, p. e1002065.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clark, M.E., A calibrated quantitative PCR based assay for measuring Wolbachia infection rates, The First Int. Wolbachia Conf. 2000, Abstracts of Papers, Boston: Int. Symbiosis Soc., 2000, p. 132.

    Google Scholar 

  • Clark, M.E., Anderson, C.L., Cande, J., and Karr, T.L., Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research, Genetics, 2005, vol. 170, pp. 1667–1675.

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark, I.E., Jan, L.Y., and Jan, Y.N., Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle, Development, 1997, vol. 124, pp. 461–470.

    CAS  PubMed  Google Scholar 

  • Clark, M.E., Veneti, Z., Bourtzis, K., and Karr, T.L., The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila, Mech. Dev. 2002, vol. 111, nos. 1–2, pp. 3–15.

    Article  CAS  PubMed  Google Scholar 

  • Clark, M.E., Veneti, Z., Bourtzis, K., and Karr, T.L., Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression, Mech. Dev., 2003, vol. 120, pp. 185–198.

    Article  CAS  PubMed  Google Scholar 

  • Cruz, J., Mané-Padròs, D., Belleés, X., and Martìn, D. Functions of the ecdysone receptor isoform-A in the hemimetabolous insect Blattella germanica revealed by systemic RNAi in vivo, Dev. Biol., 2006, vol. 297, no. 1, pp. 158–171.

    Article  CAS  PubMed  Google Scholar 

  • Dansereau, D.A. and Lasko, P., The development of germline stem cells in Drosophila, Methods Mol. Biol., 2008, vol. 450, pp. 3–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Crespigny, F.E., Pitt, T.D., and Wedell, N., Increased male mating rate in Drosophila is associated with Wolbachia infection, J. Evol. Biol., 2006, vol. 19, pp. 1964–1972.

    Article  PubMed  Google Scholar 

  • Dedeine, F., Boulétreau, M., and Vavre, F., Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida, Heredity, 2005, vol. 95, pp. 394–400.

    Article  CAS  PubMed  Google Scholar 

  • Dedeine, F., Vavre, F., Fleury, F., et al., Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 9, no. 11, pp. 6247–6252.

    Article  Google Scholar 

  • Dedeine, F., Vavre, F., Shoemaker, D.D., and Boulétreau, M., Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida, Evolution, 2004, vol. 58, no. 10, pp. 2167–2174.

    Article  PubMed  Google Scholar 

  • Dobson, S.L., Rattanadechakul, W., and Marsland, E.J., Fitness advantage and cytoplasmic incompatibility in Wolbachia single-and superinfected Aedes albopictus, Heredity, 2004, vol. 93, pp. 135–142.

    Article  CAS  PubMed  Google Scholar 

  • Dudkina, N.V., Voronin, D.A., and Kiseleva, E.V., Structure and distribution of symbiotic bacterium Wolbachia in early embryos and ovaries of Drosophila melanogaster and D. simulans, Tsitologiya, 2004, vol. 46, no. 3, pp. 208–220.

    CAS  Google Scholar 

  • Dunbar, H.E., Wilson, A.C.C., Ferguson, N.R., and Moran, N.A., Aphid thermal tolerance is governed by a point mutation in bacterial symbionts, PLoS Biol., 2007, vol. 5, p. e96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dyson, E.A. and Gregory, D.D., Persistence of an extreme sexratio bias in a natural population, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, no. 17, pp. 6520–6523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elnagdy, S., Messing, S., and Majerus, M.E.N., Two strains of male-killing Wolbachia in a ladybird, Coccinella undecimpunctata, from a hot climate, PLoS One, 2013, vol. 8, no. 1, p. e54218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fast, E., Toomey, M., Panaram, K., et al., Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche, Science, 2011, vol. 334, pp. 990–992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferree, P.M., Frydman, H.M., Li, J.M., et al., Wolbachia utilizes host microtubules and dynein for anterior localization in the Drosophila oocyte, PLoS Pathog., 2005, vol. 1, p. e14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fleury, F., Vavre, F., Ris, N., et al., Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in Drosphila parasitoid Leptopilina heterotoma, Parasitology, 2000, vol. 121, no. 05, pp. 493–500.

    Article  PubMed  Google Scholar 

  • Frydman, H.M., Li, J.M., Robson, D.N., and Wieschaus, E., Somatic stem cell niche tropism in Wolbachia, Nature, 2006, vol. 441, pp. 509–512.

    Article  CAS  PubMed  Google Scholar 

  • Fuller, M.T., Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis, Semin. Cell Dev. Biol., 1998, vol. 9, pp. 433–444.

    Article  CAS  PubMed  Google Scholar 

  • Ganter, G.K., Walton, K.L., Merriman, J.O., et al., Increased male-male courtship in ecdysone receptor deficient adult flies, Behav. Genet., 2007, vol. 37, pp. 507–512.

    Article  PubMed  Google Scholar 

  • Gill, A.C., Darby, A.C., and Makepeace, B.L., Iron necessity: the secret of Wolbachia’s success? PLoS Negl. Trop. Dis., 2014, vol. 8, no. 10, p. e3224.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Glaser, R.L. and Meola, M.A., The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile Virus infection, PLoS One, 2010, vol. 5, no. 8, p. e11977.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez-Reyes, A., Elliott, H., and St. Johnston, D., Polarization of both major body axes in Drosophila by gurkentorpedo signaling, Nature, 1995, vol. 375, pp. 654–658.

    Article  CAS  PubMed  Google Scholar 

  • Goryacheva, I.I. and Andrianov, B.V., Biological effects of Wolbachia pipientis: elucidation of genetic mechanisms, Biol. Bull. Rev., 2015, vol. 5, no. 2, pp. 109–118.

    Article  Google Scholar 

  • Goryacheva, I.I., Gorelova, T.V., and Andrianov, B.V., Drosophila melanogaster cell culture as an experimental model to study recombination in Wolbachia pipientis, Russ. J. Genet., 2015, vol. 51, no. 12, pp. 1159–1164.

    Article  CAS  Google Scholar 

  • Harris, H.L. and Braig, H.R., Sperm chromatin remodeling and Wolbachia-induced cytoplasmic incompatibility in Drosophila, Biochem. Cell Biol., 2003, vol. 81, pp. 229–240.

    Article  CAS  PubMed  Google Scholar 

  • Hedges, L.M., Brownlie, J.C., O’Neill, S.L., and Johnson, K.N., Wolbachia and virus protection in insects, Science, 2008, vol. 322, p. 702.

    Article  CAS  PubMed  Google Scholar 

  • Hertig, M., The rickettsia, Wolbachia pipientis (gen. et sp. n.) and associated inclusions of the mosquito, Culex pipiens, Parasitology, 1936, vol. 28, pp. 453–486.

    Article  Google Scholar 

  • Hilgenboecker, K., Hammerstein, P., Schlattmann, P., et al., How many species are infected with Wolbachia? A statistical analysis of current data, FEMS Microbiol. Lett., 2008, vol. 281, no. 2, pp. 215–220.

    Article  CAS  Google Scholar 

  • Hiroki, M., Kato, Y., Kamito, T., et al., Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae), Naturwissenschaften, 2002, vol. 89, pp. 167–170.

    CAS  Google Scholar 

  • Hoffmann, A.A., Hercus, M., and Dagher, H., Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster, Genetics, 1998, vol. 148, pp. 221–231.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann, A.A., Turelli, M., and Harshman, L.G., Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans, Genetics, 1990, vol. 126, pp. 933–948.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hornett, E.A., Moran, B., Reynolds, L.A., et al., The evolution of sex ratio distorter suppression affects a 25 cM genomic region in the butterfly Hypolimnas bolina, PLoS Genet., 2014, vol. 10, no. 12, p. e1004822.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hosokawa, T., Koga, R., Kikuchi, Y., et al., Wolbachia as a bacteriocyte-associated nutritional mutualist, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 2, pp. 769–774.

    Article  CAS  PubMed  Google Scholar 

  • Hurst, G.D.D., Johnson, A.P., Schulenburg, H.J.G., and Fuyama, Y., Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density, Genetics, 2000, vol. 156, pp. 699–709.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst, G.D.D., Majerus, M.E.N., and Walker, L.E., Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae), Heredity, 1992, vol. 69, pp. 84–91.

    Article  Google Scholar 

  • Hussain, Z.G., O’Neill, M., and Asgari, S.L., Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, no. 25, pp. 10276–10281.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ikeya, T., Broughton, S., Alic, N., et al., The endosymbiont Wolbachia increases insulin/IGF-like signaling in Drosophila, Proc. Biol. Sci., 2009, vol. 276, pp. 3799–3807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiggins, F.M., Hurst, G.D.D., and Majerus, M.E.N., Sex ratio distortion in Acrea encedon (Lepidoptera: Nymphalidae) is caused by a male-killing bacterium, Heredity, 1998, vol. 81, pp. 87–91.

    Article  Google Scholar 

  • Jiggins, F.M., Hurst, G.D.D., and Majerus, M.E.N., Sexratiodistorting Wolbachia causes sex-role reversal in its butterfly host, Proc. R. Soc. Lond. B, 2000, vol. 267, pp. 69–73.

    Article  CAS  Google Scholar 

  • Kageyama, D., Hoshizaki, S., and Ishikawa, Y., Femalebiased sex ratio in the Asian corn borer, Ostrinia furnacalis: evidence for the occurrence of feminizing bacteria in an insect, Heredity, 1998, vol. 81, pp. 311–316.

    Article  Google Scholar 

  • Kageyama, D., Nishimura, G., Hoshizaki, S., and Ishikawa, Y., Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae), Heredity, 2002, vol. 88, pp. 444–449.

    Article  CAS  PubMed  Google Scholar 

  • Kambris, Z., Blagborough, A.M., Pinto, S.B., et al., Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae, PLoS Pathog., 2010, no. 6, p. e1001143.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kambris, Z., Cook, P.E., Phuc, H.K., and Sinkins, S.P., Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes, Science, 2009, vol. 326, pp. 134–136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King, R.C., Ovarian Development in Drosophila melanogaster, New York: Academic, 1970.

    Google Scholar 

  • Klasson, L., Walker, T., Sebaihia, M., et al., Genome evolution of Wolbachia strain wPip from the Culex pipiens group, Mol. Biol. Evol., 2008, vol. 25, no. 9, pp. 1877–1887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klasson, L., Westberg, J., Sapountzis, P., et al., The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 14, pp. 5725–5730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kremer, N., Voronin, D., Charif, D., et al., Wolbachia interferes with ferritin expression and iron metabolism in insects, PLoS Pathog., 2009, vol. 5, no. 10, p. e1000630.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin, M.Q. and Rikihisa, Y., Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid a biosynthesis and incorporate cholesterol for their survival, Infect. Immun., 2003, vol. 71, pp. 5324–5331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobbia, S., Niitsu, S., and Fujiwara, H., Female-specific wing degeneration caused by ecdysteroid in the tussock moth, Orgyia recens: hormonal and developmental regulation of sexual dimorphism, J. Insect Sci., 2003, vol. 3, pp. 1–7.

    Article  Google Scholar 

  • Louis, C. and Nigro, L., Ultrastructural evidence of Wolbachia rickettsiales in Drosophila simulans and their relationships with unidirectional cross-incompatibility, J. Invert. Pathol., 1989, vol. 54, pp. 39–44.

    Article  Google Scholar 

  • Lus, Ya.Ya., Some regularities of reproduction of Adalia bipunctata L. populations. Male-less families in populations, Dokl. Akad. Nauk SSSR, 1947, vol. 57, no. 9, pp. 951–954.

    Google Scholar 

  • Malloch, G. and Fenton, B., Super-infections of Wolbachia in byturid beetles and evidence for genetic transfer between A and B super-groups of Wolbachia, Mol. Ecol., 2005, vol. 14, pp. 627–637.

    Article  CAS  PubMed  Google Scholar 

  • Martinez, J., Longdon, B., Bauer, S., et al., Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains, PLoS Pathog., 2014, vol. 10, no. 9, p. e1004369.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moreira, L.A., Iturbe-Ormaetxe, I., Jeffery, J.A., et al., A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium, Cell, 2009, vol. 139, pp. 1268–1278.

    Google Scholar 

  • Narita, S., Kageyama, D., Nomura, M., and Fukatsu, T., Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development, Appl. Environ. Microbiol., 2007, pp. 4332–4341.

    Google Scholar 

  • Navarro, C., Puthalakath, H., Adams, J.M., et al., Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate, Nat. Cell. Biol., 2004, vol. 6, pp. 427–435.

    Article  CAS  PubMed  Google Scholar 

  • Negri, I., Wolbachia as an “infectious” extrinsic factor manipulating host signaling pathways, Front. Endocrinol., 2012, vol. 2, art. ID 115.

  • Negri, I., Franchini, A., Mandrioli, M., et al., The gonads of Zyginidia pullula males feminized by Wolbachia pipientis, Bull. Insectol., 2008, vol. 61, no. 1, pp. 213–214.

    Google Scholar 

  • Negri, I., Pelleccia, M., Mazzoglio, P.J., et al., Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/X0 sex determination system, Proc. R. Soc. Lond. B, 2006, vol. 273, pp. 2409–2416.

    Article  CAS  Google Scholar 

  • Nikoh, N., Hosokawa, T., Moriyama, M., et al., Evolutionary origin of insect–Wolbachia nutritional mutualism, Proc. Natl. Acad. Sci. U.S.A., 2014, vol. 111, no. 28, pp. 10257–10262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noguchi, T., Lenartowska, M., Rogat, A.D., et al., Proper cellular reorganization during Drosophila spermatid individualization depends on actin structures composed of two domains, bundles and meshwork, that are differentially regulated and have different functions, Mol. Biol. Cell, 2008, vol. 19, no. 6, pp. 2363–2372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osborne, S.E., Leong, Y.S., O’Neill, S.L., and Johnson, K.N., Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans, PLoS Pathog., 2009, vol. 5, p. e1000656.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pan, X., Zhou, G., Wu, J., et al., Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, no. 1, pp. E23–E31.

    Article  PubMed  Google Scholar 

  • Pannebakker, B.A., Loppin, B., Elemans, C.P., et al., Parasitic inhibition of cell death facilitates symbiosis, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, pp. 213–215.

    Article  CAS  PubMed  Google Scholar 

  • Panteleev, D.Yu., Goryacheva, I.I., Andrianov, B.V., Reznik, N.L., Lazebny, O.E., and Kulikov, A.M., The endosymbiotic bacterium Wolbachia enhances the nonspecific resistance to insect pathogens and alters behavior of Drosophila melanogaster, Russ. J. Genet., 2007, vol. 43, no. 9, pp. 1066–1069.

    Article  CAS  Google Scholar 

  • Poinsot, D., Charlat, S., and Mercot, H., On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts, BioEssays, 2003, vol. 25, pp. 259–265.

    Article  PubMed  Google Scholar 

  • Presgraves, D.C., A genetic test of the mechanism of Wolbachia- induced cytoplasmic incompatibility in Drosophila, Genetics, 2000, vol. 154, pp. 771–776.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raquin, V., Moro, C.V., Saucereau, Y., et al., Native Wolbachia from Aedes albopictus blocks chikungunya virus infection in cellulo, PLoS One, 2015, vol. 4, p. e0125066.

    Article  CAS  Google Scholar 

  • Reed, K.M. and Werren, J.H., Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events, Mol. Reprod. Dev., 1995, vol. 40, pp. 408–418.

    Article  CAS  PubMed  Google Scholar 

  • Reuter, M. and Keller, L., High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta, Mol. Biol. Evol., 2003, vol. 20, pp. 748–753.

    Article  CAS  PubMed  Google Scholar 

  • Richard, D.S., Rybczynski, R., Wilson, T.G., et al., Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary, J. Insect Physiol., 2005, vol. 51, pp. 455–464.

    Article  CAS  PubMed  Google Scholar 

  • Rij van, R.P., Saleh, M.C., Berry, B., et al., The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster, Genes Dev., 2006, vol. 20, pp. 2985–2995.

    Article  CAS  Google Scholar 

  • Riparbelli, M.G., Giordano, R., and Callaini, G., Effects of Wolbachia on sperm maturation and architecture in Drosophila simulans Riverside, Mech. Dev., 2007, vol. 124, pp. 699–714.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, J.T., Wojcik, E.J., Sanders, M.A., et al., Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila, J. Cell Biol., 1999, vol. 146, pp. 597–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset, F., Bouchon, D., Pintureau, B., et al., Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods, Proc. R. Soc. Lond. B, 1992, vol. 250, no. 1328, pp. 91–98.

    Article  CAS  Google Scholar 

  • Sakamoto, H., Kageyama, D., Hoshizaki, S., and Ishikawa, Y., Sex-specific death in the Asian corn borer moth (Ostrinia furnacalis) infected with Wolbachia occurs across larval development, Genome, 2007, vol. 50, no. 7, pp. 645–652.

    Article  PubMed  Google Scholar 

  • Serbus, L.R. and Sullivan, W., A cellular basis for Wolbachia recruitment to the host germline, PLoS Pathog., 2007, vol. 3, p. e190.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shigenobu, S., Watanabe, H., Hattori, M., et al., Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS, Nature, 2000, vol. 407, pp. 81–86.

    Article  CAS  PubMed  Google Scholar 

  • Sluder, G., Thompson, E.A., Rieder, C.L., and Miller, F.J., Nuclear envelope breakdown is under nuclear not cytoplasmic control in sea urchin zygotes, J. Cell. Biol., 1995, vol. 129, pp. 1447–1458.

    Article  CAS  PubMed  Google Scholar 

  • Snook, R.R., Cleland, S.Y., Wolfner, M.F., and Karr, T.L., Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins, Genetics, 2000, vol. 155, pp. 167–178.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stouthamer, R., Breeuwer, J.A.J., and Hurst, G.D.D., Wolbachia pipientis: microbial manipulator of arthropod reproduction, Ann. Rev. Microbiol., 1999, vol. 53, pp. 71–102.

    Article  CAS  Google Scholar 

  • Stouthamer, R. and Kazmer, J.D., Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps, Heredity, 1994, vol. 73, pp. 317–327.

    Article  Google Scholar 

  • Stouthamer, R., Luck, R.F., and Hamilton, W.D., Antibiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex, Proc. Natl. Acad. Sci. U.S.A., 1990, vol. 87, pp. 2424–2427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stouthamer, R. and Werren, J.H., Microbes associated with parthenogenesis in wasps of the genus Trichogramma, J. Invert. Pathol., 1993, vol. 61, pp. 6–9.

    Article  Google Scholar 

  • Sugimoto, T.N. and Ishikawa, Y., A male-killing Wolbachia carries a feminizing factor and associated with degradation of the sex-determining system of its host, Biol. Lett., 2012, vol. 8, pp. 412–415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teixeira, L., Ferreira, A., and Ashburner, M., The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster, PLoS Biol., 2008, vol. 6, p. e1000002.

    Article  PubMed Central  CAS  Google Scholar 

  • Theurkauf, W.E., Smiley, S., Wong, M.L., and Alberts, B.M., Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport, Development, 1992, vol. 115, pp. 923–936.

    CAS  PubMed  Google Scholar 

  • Toomey, M.E. and Frydman, H.M., Extreme divergence of Wolbachia tropism for the stem-cell-niche in the Drosophila testis, PloS Pathog., 2014, vol. 10, no. 12, p. e1004577.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toomey, M.E., Panaram, K., Fast, E.M., et al., Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, no. 26, pp. 10788–10793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tram, U. and Sullivan, W., Role of delayed nuclear envelope breakdown and mitosis in Wolbachia induced cytoplasmic incompatibility, Science, 2002, vol. 296, pp. 1124–1126.

    Article  CAS  PubMed  Google Scholar 

  • Tram, U., Ferree, P.M., and Sullivan, W., Identification of Wolbachia—host interacting factors through cytological analysis, Microbes Infect., 2003, vol. 5, no. 11, pp. 999–1011.

    Article  CAS  PubMed  Google Scholar 

  • Tram, U., Fredrick, K., Werren, J.H., and Sullivan, W., Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype, J. Cell Sci., 2006, vol. 119, pp. 3655–3663.

    Article  CAS  PubMed  Google Scholar 

  • Truman, J.W., Steroid hormone secretion in insects comes of age, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 24, pp. 8909–8910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veneti, Z., Clark, M.E., Karr, T.L., et al., Heads or tails: host-parasite interactions in the Drosophila–Wolbachia system, App. Env. Microbiol., 2004, vol. 70, no. 9, pp. 5366–5372.

    Article  CAS  Google Scholar 

  • Verne, S., Johnson, M., Bouchon, D., and Grandjean, F., Evidence for recombination between feminizing Wolbachia in the isopod genus Armadillidium, Gene, 2007, vol. 397, pp. 58–66.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, A.R., Turelli, M., Harcombe, W.R., et al., From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila, PLoS Biol., 2007, vol. 5, p. e114.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Werren, J.H. and Bartos, J.D., Recombination in Wolbachia, Curr. Biol., 2001, vol. 11, pp. 431–435.

    Article  CAS  PubMed  Google Scholar 

  • Werren, J.H., Hurst, G.D.D., Zhang, W., et al., Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata), J. Bacteriol., 1994, vol. 176, pp. 388–394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong, Z.S., Hedges, L.M., Brownlie, J.C., and Johnson, K.N., Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila, PLoS One, 2011, vol. 6, p. e25430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, M., Sun, L.V., Vamathevan, J., et al., Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements, PLoS Biol., 2004, vol. 2, p. e69.

    Article  PubMed  PubMed Central  Google Scholar 

  • **, Z., Khoo, C.C., and Dobson, S.L., Wolbachia establishment and invasion in an Aedes aegypti laboratory population, Science, 2005, vol. 310, pp. 326–328.

    Article  CAS  PubMed  Google Scholar 

  • Yang, X.H., Zhu, D.H., Liu, Z., et al., High levels of multiple infections, recombination and horizontal transmission of Wolbachia in the Andricus mukaigawae (Hymenoptera; Cynipidae) communities, PLoS One, 2013, vol. 8, no. 11, p. e78970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye, Y.H., Woolfit, M., Rancés, E., et al., Wolbachia-associated bacterial protection in the mosquito Aedes aegypti, PLoS Negl. Trop. Dis., 2013, vol. 7, no. 8, p. e2362.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yen, J.H. and Barr, A.R., New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L., Nature, 1971, vol. 232, pp. 657–658.

    Article  CAS  PubMed  Google Scholar 

  • Zabalou, S., Apostolaki, A., Pattas, S., et al., Multiple rescue factors within a Wolbachia strain, Genetics, 2008, vol. 178, pp. 2145–2160.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zélé, F., Nicot, A., Duron, O., and Rivero, A., Infection with Wolbachia protects mosquitoes against Plasmodium-induced mortality in a natural system, J. Evol. Biol., 2012, vol. 25, pp. 1243–1252.

    Article  PubMed  Google Scholar 

  • Zakharov, I.A., Goryacheva, I.I., Shaikevich, E.V., and Dorzhu, Ch.M., Distribution of cytoplasmically inherited bacteria of the genus Spiroplasma causing female bias in Eurasian populations of Adalia bipunctata L., Russ. J. Genet., 2000, vol. 36, no. 2, pp. 135–137.

    CAS  Google Scholar 

  • Zug, R. and Hammerstein, P., Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected, PLoS One, 2012, vol. 7, no. 6, p. e38544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 117971, Russia

    I. I. Goryacheva & B. V. Andrianov

Authors
  1. I. I. Goryacheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. V. Andrianov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. I. Goryacheva.

Additional information

Original Russian Text © I.I. Goryacheva, B.V. Andrianov, 2016, published in Uspekhi Sovremennoi Biologii, 2016, Vol. 136, No. 3, pp. 247–265.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goryacheva, I.I., Andrianov, B.V. Biological effects of the symbiosis between insects and intracellular bacteria Wolbachia pipientis . Biol Bull Rev 6, 530–544 (2016). https://doi.org/10.1134/S2079086416060037

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086416060037

Keywords

Search

Navigation