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

Microbial Ecology

Volumn 61, Issue 2, 2011, Pages 254-263

  Tabata, Jun ^a   Hattori, Yuuki ^b   Sakamoto, Hironori ^a,b   Yukuhiro, Fumiko ^c   Fujii, Takeshi ^b   Kugimiya, Soichi ^a   Mochizuki, Atsushi ^a   Ishikawa, Yukio ^b   Kageyama, Daisuke ^c  

^a NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ANIMAL; ARTICLE; BACTERIAL GENE; CLASSIFICATION; FEMALE; GENETICS; INHERITANCE; MALE; MICROBIOLOGY; MOTH; OVARY; PATHOGENICITY; PHYLOGENY; SEX RATIO; SPIROPLASMA; ULTRASTRUCTURE;

ANIMALS; FEMALE; GENES, BACTERIAL; INHERITANCE PATTERNS; MALE; MOTHS; OVARY; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEX RATIO; SPIROPLASMA;

ARTHROPODA; BACTERIA (MICROORGANISMS); IXODIDA; LEPIDOPTERA; OSTRINIA; OSTRINIA ZAGULIAEVI; SPIROPLASMA; SPIROPLASMA IXODETIS; WOLBACHIA;

EID: 79951513847     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-010-9799-y     Document Type: Article

References (53)

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: 2629-2635.
2. Amikam D, Glaser G, Razin S (1984) Mycoplasmas (Mollicutes) have a low number of rRNA genes. J Bacteriol 158: 376-378.
3. Anbutsu H, Fukatsu T (2003) Population dynamics of male-killing and non-male-killing spiroplasmas in Drosophila melanogaster. Appl Environ Microbiol 69: 1428-1434.
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: 6053-6059.
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: 2373-2378.
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: 278-288.
7. Charlat S, Davies N, Roderick GK, Hurst GD (2007) Disrupting the timing of Wolbachia-induced male killing. Biol Lett 3: 154-156.
8. Cosby LD, Criddle CS (2003) Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34: 790-802.
9. Counce SJ, Poulson DF (1962) Developmental effects of the sex ratio agent in embryos at Drosophila willistoni. J Exp Zool 151: 12-31.
10. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40: 297-331.
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: 27.
12. Enigl M, Schausberger P (2007) Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Exp Appl Acarol 42: 75-85.
13. Fukatsu T, Nikoh N (2000) Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl Environ Microbiol 66: 643-650.
14. Fukatsu T, Tsuchida T, Nikoh N, Koga R (2001) Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 67: 1284-1291.
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: 893-918.
16. Goodacre SL, Martin OY, Thomas CF, Hewitt GM (2006) Wolbachia and other endosymbiont infections in spiders. Mol Ecol 15: 517-527.
17. Haselkorn TS, Markow TA, Moran NA (2009) Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18: 1294-1305.
18. Hattori I, Mutuura A (1987) Identification of Japanese species belonging to the genus Ostrinia with the host relationships. Plant Prot 41: 24-31.
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: 1753-1756.
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: 133-139.
21. Hurst GDD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6: 329-336.
22. Hurst GDD, Majerus MEN (1993) Why do maternally inherited microorganisms kill males? Heredity 71: 81-95.
23. Hurst LD (1991) The incidences and evolution of cytoplasmic male killers. Proc R Soc Lond B 244: 91-99.
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: 237-244.
25. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212-215.
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: 439-446.
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: 333-337.
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: 6667-6673.
29. Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y (2002) Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity 88: 444-449.
30. Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y (2003) Two kinds of sex ratio distorters in a moth, Ostrinia scapulalis. Genome 46: 974-982.
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: 79-83.
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: 983-989.
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: 251-258.
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: 405-412.
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: 551-555.
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 295-319.
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: 2699-2702.
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: 335-339.
39. Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11: 2983-3002.
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: 645-652.
41. Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53: 71-102.
42. Swofford DL (2001) 'PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4. 0.
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.
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: 566-574.
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).
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: 4673-4680.
47. Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132: 757-765.
48. Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71: 239-256.
49. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587-609.
50. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
51. Whitcomb RF, Tully JG (1979) The mycoplasmas, vol 3. Academic, New York.
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 175-208.
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: e12149.