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Microbial Ecology

, Volume 61, Issue 2, pp 254–263 | Cite as

Male Killing and Incomplete Inheritance of a Novel Spiroplasma in the Moth Ostrinia zaguliaevi

  • Jun Tabata
  • Yuuki Hattori
  • Hironori Sakamoto
  • Fumiko Yukuhiro
  • Takeshi Fujii
  • Soichi Kugimiya
  • Atsushi Mochizuki
  • Yukio Ishikawa
  • Daisuke Kageyama
Host Microbe Interactions

Abstract

Bacteria of the genus Spiroplasma are widely found in plants and arthropods. Some of the maternally transmitted Spiroplasma endosymbionts in arthropods are known to kill young male hosts (male killing). Here, we describe a new case of Spiroplasma-induced male killing in a moth, Ostrinia zaguliaevi. The all-female trait caused by Spiroplasma was maternally inherited for more than 11 generations but was spontaneously lost in several lineages. Antibiotic treatment eliminated the Spiroplasma infection and restored the 1:1 sex ratio. The survival rates and presence/absence of the W chromosome in the embryonic and larval stages of O. zaguliaevi showed that males were selectively killed, exclusively during late embryogenesis in all-female broods. Based on phylogenetic analyses of 16S rRNA, dnaA and rpoB gene sequences, the causative bacteria were identified as Spiroplasma belonging to the tick symbiont Spiroplasma ixodetis clade. Electron microscopy confirmed bacterial structures in the follicle cells and follicular sheath of adult females. Although many congeneric Ostrinia moths harbor another sex ratio-distorting bacterium (Wolbachia), only O. zaguliaevi harbors Spiroplasma.

Keywords

Follicle Cell rpoB Gene Wolbachia Infection Ladybird Beetle Male Host 
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.

Notes

Acknowledgments

We thank Drs. Sadahiro Tatsuki and Sugihiko Hoshizaki (The University of Tokyo) for advice and technical assistance on the study. JT acknowledges a grant-in-aid from JSPS Excellent Young Researchers Overseas Visit Program (no. 21-7080).

References

  1. 1.
    Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186:2629–2635CrossRefPubMedGoogle Scholar
  2. 2.
    Amikam D, Glaser G, Razin S (1984) Mycoplasmas (Mollicutes) have a low number of rRNA genes. J Bacteriol 158:376–378PubMedGoogle Scholar
  3. 3.
    Anbutsu H, Fukatsu T (2003) Population dynamics of male-killing and non-male-killing spiroplasmas in Drosophila melanogaster. Appl Environ Microbiol 69:1428–1434CrossRefPubMedGoogle Scholar
  4. 4.
    Anbutsu H, Goto S, Fukatsu T (2008) High and low temperatures differently affect infection density and vertical transmission of male-killing Spiroplasma symbionts in Drosophila hosts. Appl Environ Microbiol 74:6053–6059CrossRefPubMedGoogle Scholar
  5. 5.
    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
  6. 6.
    Case RJ, Boucher Y, Dahllof I, Holmstrom C, Doolittle WF, Kjelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288CrossRefPubMedGoogle Scholar
  7. 7.
    Charlat S, Davies N, Roderick GK, Hurst GD (2007) Disrupting the timing of Wolbachia-induced male killing. Biol Lett 3:154–156CrossRefPubMedGoogle Scholar
  8. 8.
    Cosby LD, Criddle CS (2003) Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34:790–802Google Scholar
  9. 9.
    Counce SJ, Poulson DF (1962) Developmental effects of the sex ratio agent in embryos at Drosophila willistoni. J Exp Zool 151:12–31CrossRefGoogle Scholar
  10. 10.
    Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331CrossRefGoogle Scholar
  11. 11.
    Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27CrossRefPubMedGoogle Scholar
  12. 12.
    Enigl M, Schausberger P (2007) Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Exp Appl Acarol 42:75–85CrossRefPubMedGoogle Scholar
  13. 13.
    Fukatsu T, Nikoh N (2000) Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl Environ Microbiol 66:643–650CrossRefPubMedGoogle Scholar
  14. 14.
    Fukatsu T, Tsuchida T, Nikoh N, Koga R (2001) Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 67:1284–1291CrossRefPubMedGoogle Scholar
  15. 15.
    Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J, Williamson DL (2004) The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Syst Evol Microbiol 54:893–918CrossRefPubMedGoogle Scholar
  16. 16.
    Goodacre SL, Martin OY, Thomas CF, Hewitt GM (2006) Wolbachia and other endosymbiont infections in spiders. Mol Ecol 15:517–527CrossRefPubMedGoogle Scholar
  17. 17.
    Haselkorn TS, Markow TA, Moran NA (2009) Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18:1294–1305CrossRefPubMedGoogle Scholar
  18. 18.
    Hattori I, Mutuura A (1987) Identification of Japanese species belonging to the genus Ostrinia with the host relationships. Plant Prot 41:24–31Google Scholar
  19. 19.
    Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756CrossRefGoogle Scholar
  20. 20.
    Hurst GDD, Graf von der Schulenburg JH, Majerus TMO, Bertrand D, Zakharov IA, Baungaard J, Völkl W, Stouthamer R, Majerus MEN (1999) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol 8:133–139CrossRefPubMedGoogle Scholar
  21. 21.
    Hurst GDD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6:329–336CrossRefPubMedGoogle Scholar
  22. 22.
    Hurst GDD, Majerus MEN (1993) Why do maternally inherited microorganisms kill males? Heredity 71:81–95CrossRefGoogle Scholar
  23. 23.
    Hurst LD (1991) The incidences and evolution of cytoplasmic male killers. Proc R Soc Lond B 244:91–99CrossRefGoogle Scholar
  24. 24.
    Ishikawa Y, Takanashi T, Kim C, Hoshizaki S, Tatsuki S, Huang Y (1999) Ostrinia spp. in Japan: their host plants and sex pheromones. Entomol Exp Appl 91:237–244CrossRefGoogle Scholar
  25. 25.
    Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215CrossRefPubMedGoogle Scholar
  26. 26.
    Jiggins FM, Hurst GDD, Jiggins CD, Von der Schulenburg JHG, Majerus MEN (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology 120:439–446CrossRefPubMedGoogle Scholar
  27. 27.
    Kageyama D, Anbutsu H, Shimada M, Fukatsu T (2007) Spiroplasma infection causes either early or late male killing in Drosophila, depending on maternal host age. Naturwissenschaften 94:333–337CrossRefPubMedGoogle Scholar
  28. 28.
    Kageyama D, Anbutsu H, Watada M, Hosokawa T, Shimada M, Fukatsu T (2006) Prevalence of a non-male-killing spiroplasma in natural populations of Drosophila hydei. Appl Environ Microbiol 72:6667–6673CrossRefPubMedGoogle Scholar
  29. 29.
    Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y (2002) Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity 88:444–449CrossRefPubMedGoogle Scholar
  30. 30.
    Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y (2003) Two kinds of sex ratio distorters in a moth, Ostrinia scapulalis. Genome 46:974–982CrossRefPubMedGoogle Scholar
  31. 31.
    Kageyama D, Nishimura G, Ohno S, Takanashi T, Hoshizaki S, Ishikawa Y (2004) Wolbachia infection and an all-female trait in Ostrinia orientalis and Ostrinia zaguliaevi. Entomol Exp Appl 111:79–83CrossRefGoogle Scholar
  32. 32.
    Kageyama D, Ohno S, Hoshizaki S, Ishikawa Y (2003) Sexual mosaics induced by tetracycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis. Genome 46:983–989CrossRefPubMedGoogle Scholar
  33. 33.
    Kageyama D, Traut W (2004) Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc R Soc Lond B 271:251–258CrossRefGoogle Scholar
  34. 34.
    Kim C, Hoshizaki S, Huang Y, Tatsuki S, Ishikawa Y (1999) Usefulness of mitochondrial COII gene sequences in examining phylogenetic relationships in the Asian corn borer, Ostrinia furnacalis, and allied species (Lepidoptera: Pyralidae). Appl Entomol Zool 34:405–412Google Scholar
  35. 35.
    Majerus TMO, Graf von der Schulenburg JH, Majerus MEN, Hurst GDD (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8:551–555CrossRefPubMedGoogle Scholar
  36. 36.
    Narita S, Kageyama D (2008) Wolbachia-induced sex reversal in Lepidoptera. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 3. CRC Press, Boca Raton, pp 295–319CrossRefGoogle Scholar
  37. 37.
    O’Neil SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702CrossRefGoogle Scholar
  38. 38.
    Osaka R, Nomura M, Watada M, Kageyama D (2008) Negative effects of low temperatures on the vertical transmission and infection density of a spiroplasma endosymbiont in Drosophila hydei. Curr Microbiol 57:335–339CrossRefPubMedGoogle Scholar
  39. 39.
    Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11:2983–3002CrossRefPubMedGoogle Scholar
  40. 40.
    Sakamoto H, Kageyama D, Hoshizaki S, Ishikawa Y (2007) Sex-specific death in the Asian corn borer moth (Ostrinia furnacalis) infected with Wolbachia occurs across larval development. Genome 50:645–652CrossRefPubMedGoogle Scholar
  41. 41.
    Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102CrossRefPubMedGoogle Scholar
  42. 42.
    Swofford DL (2001) ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4.0.Google Scholar
  43. 43.
    Tabata J (2010) Studies on inter- and intra-specific variations and their mode of inheritance in sex pheromone production and response of moths. Ph.D. dissertation, The University of Tokyo.Google Scholar
  44. 44.
    Tabata J, Huang Y, Ohno S, Yoshiyasu Y, Sugie H, Tatsuki S, Ishikawa Y (2008) Sex pheromone of Ostrinia sp. newly found on the leopard plant Farfugium japonicum. J Appl Entomol 132:566–574CrossRefGoogle Scholar
  45. 45.
    Tabata J, Ishikawa Y (2011) Genetic basis regulating the sex pheromone blend in Ostrinia zealis (Lepidoptera: Crambidae) and its allies inferred from crossing experiments. Ann Entomol Soc Am (in press)Google Scholar
  46. 46.
    Thompson JD, Higgins DG, Gibson TJ (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 22:4673–4680CrossRefPubMedGoogle Scholar
  47. 47.
    Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757–765CrossRefPubMedGoogle Scholar
  48. 48.
    Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71:239–256CrossRefPubMedGoogle Scholar
  49. 49.
    Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609CrossRefPubMedGoogle Scholar
  50. 50.
    Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751CrossRefPubMedGoogle Scholar
  51. 51.
    Whitcomb RF, Tully JG (1979) The mycoplasmas, vol 3. Academic, New YorkGoogle Scholar
  52. 52.
    Williamson DL, Poulson DF (1979) Sex ratio organisms (spiroplasmas) of Drosophila. In: Whitcomb RF, Tully JG (eds) The mycoplasmas, vol 3. Academic, New York, pp 175–208Google Scholar
  53. 53.
    Xie J, Vilchez I, Mateos M (2010) Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE 5:e12149CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Jun Tabata
    • 1
  • Yuuki Hattori
    • 2
  • Hironori Sakamoto
    • 1
    • 2
  • Fumiko Yukuhiro
    • 3
  • Takeshi Fujii
    • 2
  • Soichi Kugimiya
    • 1
  • Atsushi Mochizuki
    • 1
  • Yukio Ishikawa
    • 2
  • Daisuke Kageyama
    • 3
  1. 1.Biodiversity DivisionNational Institute for Agro-Environmental SciencesTsukubaJapan
  2. 2.Laboratory of Applied Entomology, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  3. 3.Insect-Microbe Research UnitNational Institute of Agrobiological SciencesTsukubaJapan

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