The spiroplasma heritable bacterial endosymbiont of Drosophila

Fly

Volumn 4, Issue 1, 2010, Pages 80-87

  Haselkorn, Tamaa S ^a  

^a University of California at San Diego   (United States)

Author keywords

Bacterial endosymbiont; Bacterial infection; Drosophila; Innate immunity; Spiroplasma; Wolbachia

Indexed keywords

BACTERIA (MICROORGANISMS); HEXAPODA; POSIBACTERIA; SPIROPLASMA; WOLBACHIA;

EID: 77952634358     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.4.1.10883     Document Type: Article

References (88)

1. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA. Heritable endosymbionts of Drosophila. Genetics 2006; 174:363-76.
2. Werren JH, Baldo L, Clark ME. Wolbachia: mas-ter manipulators of invertebrate biology. Nature Rev Microbiol 2008; 6:741-51.
3. Anderson RM, May RM. Coevolution of Hosts and Parasites. Parasitology 1982; 85:411-26.
4. Bull JJ, Molineux IJ, Rice WR. Selection of Benevolence in a Host-Parasite System. Evolution 1991; 45:875-82.
5. Ewald PW. Host-Parasite Relations, Vectors and the Evolution of Disease Severity. Ann Rev Ecol Sys 1983; 14:465-85.
6. O'Neill S, Hoffmann A, Werren JH. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press: New York 1997.
7. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. Wolbachia and virus protection in insects. Science 2008; 322:702.
8. Teixeira L, Ferreira A, Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 2008; 6:2.
9. Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, et al. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Path 2009; 5:1000368.
10. Ota T, Kawabe M, Oishi K, Poulson DF. Non-male-killing Spiroplasma in Drosophila hydei. J Hered 1979; 70:211-3.
11. Kageyama D, Anbutsu H, Watada M, Hosokawa T, Shimada M, Fukatsu T. Prevalence of a non-male-kill-ing Spiroplasma in natural populations of Drosophila hydei. Appl Environ Microbiol 2006; 72:6667-73.
12. Williamson DL, Poulson DF. Sex Ratio Organisms (Spiroplasma) of Drosophila in The Mycoplasmas III: Plant and Insect Mycoplasmas, Academic Press, New York 1979; 3:176-206.
13. Watts T, Haselkorn TS, Moran NA, Markow TA. Variable incidence of Spiroplasma infections in natural populations of Drosophila species. PloS One 2009; 4:5703.
14. Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J, Williamson DL. The genus Spiroplasma and its non-helical descendants: phylogenetic clas-sification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Sys Evol Microbiol 2004; 54:893-918.
15. Woese CR, Maniloff J, Zablen LB. Phylogenetic analy-sis of the mycoplasmas. Proc Natl Acad Sci USA 1980; 77:494-8.
16. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 2008; 6:27.
17. Hurst GDD, von der Schulenburg JHG, Majerus TMO, Bertrand D, Zakharov IA, Baungaard J, et al. Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol 1999; 8:133-9.
18. Majerus TMO, von der Schulenburg JHG, Majerus MEN, Hurst GDD. Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 1999; 8:551-5.
19. Tinsley MC, Majerus ME. A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 2006; 132:757-65.
20. Jiggins FM, Hurst GDD, Jiggins CD, Von der Schulenburg JHG, Majerus MEN. The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bac-terium. Parasitology 2000; 120:439-46.
21. Goodacre SL, Martin OY, Thomas CFG, Hewitt GM. Wolbachia and other endosymbiont infections in spi-ders. Mol Ecol 2006; 15:517-27.
22. Bove JM. Spiroplasma: Infections agents of plants, arthropods and vertebrates. Wiener Klinische Wochenschrift 1997; 109:604-12.
23. Nunan LM, Lightner DV, Oduori MA, Gasparich GE. Spiroplasma penaei sp nov., associated with mortalities in Penaeus vannamei, Pacific white shrimp. Int J Syst Evol Microbiol 2005; 55:2317-22.
24. Wang W, Gu W, Ding Z, Ren Y, Chen J, Hou Y. A novel Spiroplasma pathogen causing systemic infec-tion in the crayfish Procambarus clarkii (Crustacea: Decapod), in China. FEMS Microbiol Lett 2005; 249:131-7.
25. Wang W, Rong L, Gu W, Du K, Chen J. Study on experimental infections of Spiroplasma from the Chinese mitten crab in crayfish, mice and embryonated chickens. Res Microbiol 2003; 154:677-80.
26. Clark TB. Spiroplasma sp. a new pathogen in honey bees. J Invertebr Pathol 1977; 29:112-3.
27. Mouches C, Menara A, Tully JG, Rose DL, McCoy RE, Clarle-Junca P, et al. Spiroplasma apis, a new species from the honeybee (Apis mellifera). Ann Inst Microbiol (Paris) 1983; 134:383-97.
28. Heres A, Lightner DV. Phylogenetic analysis of the pathogenic bacteria Spiroplasma penaei based on mul-tilocus sequence analysis. J Invertebr Pathol 2010; 103:30-5.
29. Clark TB. Spiroplasma: Diversity of arthropod res-ervoirs and host-parasite relationships. Science 1982; 217:57-9.
30. Bove JM, Renaudin J, Saillard C, Foissac X, Garnier M. Spiroplasma citri, a plant pathogenic molligute: rela-tionships with its two hosts, the plant and the leafhop-per vector. Annu Rev Phytopathol 2003; 41:483-500.
31. Markham PG, Townsend R, Bar-Joseph M, Daniels MJ, Plaskitt A, Meddins BM. Spiroplasma are the causal agents of citrus little-leaf disease. Ann Appl Biol 1974; 78:49-57.
32. Davis RE, Worley JF, Whitcomb RF, Ishijima T, Steere R.L. Helical flilaments produced by a mycoplasma-like organism associated with corn stunt disease. Science 1972; 176:521-3.
33. Hackett KJ, Clark TB. Ecology of Spiroplasma. In: Whitcomb RF, Tully JG, eds. The Mycoplasmas, Vol V: Spiroplasma, Acholeplasmas and Mycoplasmas of Plant and Arthropods. San Diego, CA: Academic Press 1989; 113-200.
34. Calavan EC, Bove JM. Ecology of Spiroplasma citri. In: Whitcomb RF, Tully JG, eds. The Mycoplasmas, Vol V: Spiroplasma, Acholeplasmas and Mycoplasmas of Plant and Arthropods. San Diego, CA: Academic Press 1989; 425-87.
35. Ebbert MA, Nault LR. Survival in Dalbulus leafhop-per vectors improves after exposure to maize stunting pathogens. Entomologia Experimentalis Et Applicata 2001; 100:311-24.
36. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD. Male-killing Spiroplasma naturally infect-ing Drosophila melanogaster. Insect Mol Biol 2005; 14:281-7.
37. Pool JE, Wong A, Aquadro CF. Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont. Heredity 2006; 97:27-32.
38. Marques EJ, de Magalhaes LE. Drosophila Information Service 1973; 50:87.
39. Montenegro H, Hatadani LM, Medeiros HF, Klaczko LB. Male killing in three species of the tripunctata radiation of Drosophila (Diptera: Drosophilidae). J Zool Sys Evol Res 2006; 44:130-5.
40. Haselkorn TS, Markow TA, Moran NA. Multiple introductions of the Spiroplasma bacterial endosymbi-ont into Drosophila. Mol Ecol 2009; 18:1294-305.
41. Williamson DL, Sakaguchi B, Hackett KJ, Whitcomb RF, Tully JG, Carle P, et al. Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int J Syst Bacteriol 1999; 49:611-8.
42. Bentley JK, Hinds G, Hurst GD. The male-killing Spiroplasma of Drosophila nebulosa and Drosophila willistoni have identical ITS sequences. Drosophila Information Service 2002; 85:63-5.
43. Niki Y. Ultrastructural study of the Sex Ratio Organism (SRO) transmission into oocytes during oogenesis in Drosophila melanogaster. Jpn J Genet 1988; 63:11-21.
44. Ebbert MA. The interaction phenotype in the Drosophila willistoni-Spiroplasma Symbiosis. Evolution 1991; 45:971-88.
45. Anbutsu H, Goto S, Fukatsu T. High and low tem-peratures differently affect infection density and vertical transmission of male-killing Spiroplasma symbionts in Drosophila hosts. Appl Environ Microbiol 2008; 74:6053-9.
46. Montenegro H, Klaczko LB. Low temperature cure of a male killing agent in Drosophila melanogaster. J Invertebr Pathol 2003; 86:50-1.
47. Osaka R, Nomura M, Watada M, Kageyama D. Negative effects of low temperatures on the vertical transmission and infection density of a Spiroplasma endosymbiont in Drosophila hydei. Curr Microbiol 2008; 57:335-9.
48. Tamura K, Subramanian S, Kumar S. Temporal pat-terns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 2004; 21:36-44.
49. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 2007; 3:23-5.
50. Carvalho GG, da Cruz M. Transfer of the "sexratio" factor in Drosophila willistoni by ingestion. Science 1962; 138:51.
51. Williamson DL. Studies on the pathogenicity of Spiroplasma for Drosophila pseudoobscura. Annales de microbiologie 1984; 135:157-62.
52. Baldo L, Bordenstein S, Wernegreen JJ, Werren JH. Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 2006; 23:437-49.
53. Marais A, Bove JM, Renaudin J. Characterization of the recA gene regions of Spiroplasma citri and Spiroplasma melliferum. J Bacteriol 1996; 178:7003-9.
54. Marais A, Bove JM, Renaudin J. Spiroplasma citri virus SpV1-derived cloning vector: Deletion forma-tion by illegitimate and homologous recombination in a Spiroplasmal host strain which probably lacks a functional recA gene. J Bacteriol 1996; 178:862-70.
55. Anderson RM, May RM. The population dynamics of microparasites and their invertebrate hosts. Phil Trans R Soc Lond B 1981; 291:451-524.
56. Sakaguchi B, Poulson DF. Interspecific transfer of the "sex-ratio" condition from Drosophila willistoni to D. melanogaster. Genetics 1963; 48:841-61.
57. Yamada M, Nawa S, Watanabe T. A mutant of SR organism (SRO) in Drosophila that does not kill the nost males. Jpn J Genet 1982; 57.
58. Anbutsu H, Fukatsu T. Population dynamics of male-killing and non-male-killing Spiroplasma in Drosophila melanogaster. Appl Environ Microbiol 2003; 69:1428-34.
59. Williamson DL. Kinetic studies of "sex-ratio" spiro-chetes in Drosophila melanogaster Meigen females. J Invertebr Pathol 1965; 7:493-501.
60. Counce SJ, Poulson DF. Developmental effects of the sex ratio agent in embryos of Drosophila willistoni. J Exp Zool 1962; 151:17-31.
61. Koana T, Miyake T. Effects of the sex ratio organism on in vitro differentiation of Drosophila embryonic cells. Genetics 1983; 104:113-22.
62. Tsuchiyama S, Sakaguchi B, Oishi K. Analysis of gynandromorph survivals in Drosophila melanogaster infected with the male-killing SR organisms. Genetics 1978; 89:711-21.
63. Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GDD. A functional dosage compensation complex required for male killing in Drosophila. Science 2005; 307:1461-3.
64. Bentley JK, Veneti Z, Heraty J, Hurst GD. The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol 2007; 5:9.
65. Kageyama D, Anbutsu H, Shimada M, Fukatsu T. Spiroplasma infection causes either early or late male killing in Drosophila, depending on maternal host age. Die Naturwissenschaften 2007; 94:333-7.
66. Kageyama D, Anbutsu H, Shimada M, Fukatsu T. Effects of host genotype against the expression of Spiroplasma-induced male killing in Drosophila mela-nogaster. Heredity 2009; 102:475-82.
67. Oishi K. Spirochaete-mediated abnormal sex-ratio (SR) condition in Drosophila: a second virus associated with spirochaetes and its use in the study of the SR condi-tion. Genet Res 1971; 18:45-56.
68. Williamson DL. The sex-ratio spirochete in Drosophila robusta. Jpn J Genet 1969; 44:36-41.
69. Williamson DL. Atypical transovarial transmission of sex ratio spirochetes by Drosophila robusta Sturtevant. J Exp Zool 1966; 161:425-9.
70. Cohen AJ, Williamson DL, Oishi K. Spv3 Viruses of Drosophila Spiroplasma. Israel J Med Sci 1987; 23:429-33.
71. Oishi K, Poulson DF. Virus associated with Sr-Spirochetes of Drosophila nebulosa. Proc Natl Acad Sci USA 1970; 67:1565-72.
72. Oishi K, Poulson DF, Williamson DL. Virus-mediated change in clumping properties of Drosophila SR Spiroplasma. Curr Microbiol 1984; 10:153-8.
73. Sakaguchi B, Oishi K, Kobayash S. Interference between sex-ratio agents of Drosophila willistoni and Drosophila nebulosa. Science 1965; 147:160-2.
74. Hurst GDD, Anbutsu H, Kutsukake M, Fukatsu T. Hidden from the host: Spiroplasma bacteria infecting Drosophila do not cause an immune response, but are suppressed by ectopic immune activation. Insect Mol Biol 2003; 12:93-7.
75. Anbutsu H, Fukatsu T. Tissue-specific infection dynam-ics of male-killing and nonmale-killing Spiroplasma in Drosophila melanogaster. FEMS Microbiol Ecol 2006; 57:40-6.
76. Goto S, Anbutsu H, Fukatsu T. Asymmetrical interac-tions between Wolbachia and Spiroplasma endosymbi-onts coexisting in the same insect host. Appl Environ Microbiol 2006; 72:4805-10.
77. Hatcher MJ, Taneyhill DE, Dunn AM, Tofts C. Population dynamics under parasitic sex ratio distor-tion. Theor Popul Biol 1999; 56:11-28.
78. Hurst GDD, Jiggins FM. Male-killing bacteria in insects: Mechanisms, incidence and implications. Emerg Infect Dis 2000; 6:329-36.
79. Engelstadter J, Hurst GD. The impact of male-killing bacteria on host evolutionary processes. Genetics 2007; 175:245-54.
80. Malogolowkin-Cohen C, Rodrigues-Pereira MA. Sexual drive of normal and SR flies of Drosophila nebu-losa. Evolution 1975; 29:579-80.
81. Ebbert MA. Variable effects of crowding on Drosophila hosts of male-lethal and non-male-lethal Spiroplasma in laboratory populations. Heredity 1995; 74:227-40.
82. Montenegro H, Petherwick AS, Hurst GDD, Klaczko LB. Fitness effects of Wolbachia and Spiroplasma in Drosophila melanogaster. Genetica 2006; 127:207-15.
83. Oliver K, Campos J, Moran N, Hunter M. Population dynamics of defensive symbionts in aphids. Proc Biol Sci 2008; 275:293-9.
84. Chen DQ, Montllor CB, Purcell AH. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomologia Experimentalis Et Applicata 2000; 95:315-23.
85. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resis-tance to parasitic wasps. Proc Natl Acad Sci USA 2003; 100:1803-7.
86. Piel J, Hofer I, Hui DQ. Evidence for a symbiosis island involved in horizontal acquisition of pederin biosynthetic capabilities by the bacterial symbiont of Paederus fuscipes beetles. J Bacteriol 2004; 186:1280-6.
87. Markow TA, O'Grady PM. Drosophila biology in the genomic age. Genetics 2007; 177:1269-76.
88. Jaenike J, Stahlhut JK, Boelio LM, Unckless R.L. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism? Mol Ecol 2010; 19:414-25.