Novel Strain of Spiroplasma Found in Flower Bugs of the Genus Orius (Hemiptera: Anthocoridae): Transovarial Transmission, Coexistence with Wolbachia and Varied Population Density

Microbial Ecology

Volumn 67, Issue 1, 2014, Pages 219-228

  Watanabe, Masaya ^a,c   Yukuhiro, Fumiko ^a   Maeda, Taro ^a   Miura, Kazuki ^b   Kageyama, Daisuke ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b NATIONAL AGRICULTURAL RESEARCH CENTER FOR WESTERN REGION   (Japan)

^c International Apatite Co Ltd   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCORIDAE; ARTHROPODA; ASTERACEAE; ASTERALES; BACTERIA (MICROORGANISMS); BIDENS; COREOPSIS; HELIANTHUS; HEMIPTERA; MOLLICUTES; ORIUS; ORIUS MINUTUS; ORIUS NAGAII; ORIUS SAUTERI; ORIUS STRIGICOLLIS; PILOPHORUS WALSHII; SPIROPLASMA; SPIROPLASMA INSOLITUM; SPIROPLASMA IXODETIS; SPIROPLASMA POULSONII; WOLBACHIA;

BACTERIAL DNA; RNA 16S;

ANIMAL; ARTICLE; CLASSIFICATION; DNA SEQUENCE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; ISOLATION AND PURIFICATION; JAPAN; MALE; MICROBIOLOGY; PHYLOGENY; SPIROPLASMA; SYMBIOSIS; WOLBACHIA;

ANIMALS; DNA, BACTERIAL; FEMALE; HEMIPTERA; JAPAN; MALE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPIROPLASMA; SYMBIOSIS; WOLBACHIA;

EID: 84893784831     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-013-0335-8     Document Type: Article

References (52)

1. Akimoto K, Urano S, Noda T, Matuo K, Sakamaki Y, Tsuda K, Kusigemati K (2005) Comparison of the reproductive potential of three Orius species, O. strigicollis, O. sauteri, and O. minutus (Heteroptera: Anthocoridae), using eggs of the Mediterranean flour moth as a food source. Appl Entomol Zool 40: 247-255.
2. Anbutsu H, Fukatsu T (2011) Spiroplasma as a model insect endosymbiont. Environ Microbiol Rep 3: 144-153.
3. Clark TB (1977) Spiroplasma sp., a new pathogen in honeybees. J Invertebr Pathol 29: 112-113.
4. Coll M (1996) Feeding and ovipositing on plants by an omnivorous insect predator. Oecologia 105: 214-220.
5. Fast E, Toomey M, Panaram K, Desjardins D, Kolaczyk E, Frydman HM (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334: 990-992.
6. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441: 509-512.
7. Fukatsu T, Nikoh N (2000) Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl Environ Microbiol 66: 643-650.
8. Hackett KJ, Whitcomb RF, Tully JG, Rose DL, Carle P, Bové JM, Henegar RB, Clark TB, Clark EA, Konai M, Adams JR, Williamson DL (1993) Spiroplasma insolitum sp. nov., a new species of group I Spiroplasma with an unusual DNA base composition. Int J Syst Evol Microbiol 43: 272-277.
9. Hinomoto N, Nagamori S, Kakimoto K, Shimizu T, Higaki T, Muraji M, Noda T, Kawasaki K (2009) Molecular identification and evaluation of Orius species (Heteroptera: Anthocoridae) as biological control agents. JSRQ 43: 281-288.
10. Hinomoto N, Muraji M, Noda T, Shimizu T, Kawasaki K (2004) Identification of five Orius species in Japan by multiplex polymerase chain reaction. Biol Control 31: 276-279.
11. Hurst GDD, Graf von der Schulenburg JH, Majerus TMO, Bertrand D, Zakharov IA, Baungaard J, Völkl W, Stouthamer R, Majerus MEM (1999) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol 8: 133-139.
12. Jaenike J, Brekke TD (2011) Defensive endosymbionts: a cryptic trophic level in community ecology. Ecol Lett 14: 150-155.
13. Jiggins FM, Hurst GDD, Jiggins CD, Von der Schulenburg JHG, Majerus MEM (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology 120: 439-446.
14. Jung S, Lee S (2011) Phylogenetic and systematic study of Korean Orius species (Heteroptera: Anthocoridae) on the basis of molecular and morphological data. Appl Entomol Zool 46: 153-164.
15. 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.
16. Kakimoto K, Inoue H, Yoshida T (2002) Seasonal changes in population density and species composition of Orius spp. in mulberry fields. Jpn J Appl Entomol Zool 46: 209-215 (in Japanese with English summary).
17. Kiman ZB, Yeargan KV (1985) Development and reproduction of the predator Orius insidiosus (Hemiptera: Anthocoridae) reared on diets of selected plant material and arthropod prey. Ann Entomol Soc Am 78: 464-467.
18. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.
19. Koerber RT, Gasparich GE, Frana MF, Grogan WL Jr (2005) Spiroplasma atrichopogonis sp. nov., from a ceratopogonid biting midge. Int J Syst Evol Microbiol 55: 289-292.
20. 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.
21. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman & Hall, London, 532 pp.
22. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD (2005) Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 14: 281-287.
23. Mouches C, Bové JM, Tully JG, Rose DL, McCoy RE, Carle-Junca P, Garnier M, Saillard C (1983) Spiroplasma apis, a new species from the honeybee (Apis mellifera). Ann Inst Microbiol (Paris) 134A: 383-397.
24. Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, Noda H (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of Candidatus Cardinium hertigii based on detection of a new Cardinium group from biting midges. Appl Environ Microbiol 75: 6757-6763.
25. Niki Y (1988) Ultrastructural study of the sex ratio organisms (SRO) transmission into oocytes during oogenesis in Drosophila melanogaster. Jpn J Genet 63: 11-21.
26. Nunan LM, Lightner DV, Oduori MA, Gasparich GE (2005) Spiroplasma penaei sp. nov., associated with mortalities in Penaeus vannamei, Pacific white shrimp. Int J Syst Evol Microbiol 55: 2317-2322.
27. Ohno K, Takemoto H (1997) Species composition and seasonal occurrence of Orius spp. (Heteroptera: Anthocoridae), predacious natural enemies of Thrips palmi (Thysanoptera: Thripidae) in eggplant fields and surrounding habitats. Appl Entomol Zool 32: 27-35.
28. Ota T, Kawabe M, Oishi K, Poulson DF (1979) Non-male-killing spiroplasmas in Drosophila hydei. J Hered 70: 211-213.
29. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www. R-project. org/.
30. Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11: 2983-3002.
31. Saglio P, Lhospital M, Laflèche D, Dupont G, Bové JM, Tully JG, Freundt EA (1973) Spiroplasma citri gen. and sp. n.: a mycoplasma-like organism associated with stubborn disease of citrus. Int J Syst Bacteriol 23: 191-204.
32. Saillard C, Vignault JC, Bove JM, Raie A, Tully JG, Williamson DL, Fos A, Garnier M, Gadeau A, Carle P, Whitcomb RF (1987) Spiroplasma phoeniceum sp. nov., a new plant-pathogenic species from Syria. Int J Syst Bacteriol 37: 106-115.
33. Sokolova MI, Zinkevich NS, Zakharov IA (2002) Bacteria in ovarioles of females from maleless families of ladybird beetles Adaliabipunctata L. (Coleoptera: Coccinellidae) naturally infected with Rickettsia, Wolbachia, and Spiroplasma. J Invertebr Pathol 79: 72-79.
34. Tabata J, Hattori Y, Sakamoto H, Yukuhiro F, Fujii T, Kugimiya S, Mochizuki A, Ishikawa Y, Kageyama D (2011) Male killing and incomplete inheritance of a novel Spiroplasma in the moth Ostriniazaguliaevi. Microb Ecol 61: 254-263.
35. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
36. 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.
37. Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132: 757-765.
38. Trachtenberg S (2004) Shaping and moving a Spiroplasma. J Mol Microbiol Biotechnol 7: 78-87.
39. Tully JG, Rose DL, Yunker CE, Carle P, Bové JM, Williamson DL, Whitcomb RF (1995) Spiroplasma ixodetis sp. nov., a new species from Ixodes pacificus ticks collected in Oregon. Int J Syst Bacteriol 45: 23-28.
40. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71-W74. doi: 10. 1093/nar/gkm306.
41. Ventura IM, Martins AB, Lyra ML, Andrade CA, Carvalho KA, Klaczko LB (2012) Spiroplasma in Drosophila melanogaster populations: prevalence, male-killing, molecular identification, and no association with Wolbachia. Microb Ecol 64: 794-801.
42. Xie J, Tiner B, Vilchez I, Mateos M (2011) Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol Ecol 53: 1065-1079.
43. 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.
44. Watanabe M, Miura K, Hunter MS, Wajnberg E (2011) Superinfection of cytoplasmic incompatibility-inducing Wolbachia is not additive in Orius strigicollis (Hemiptera: Anthocoridae). Heredity 106: 642-648.
45. Watanabe M, Tagami Y, Miura K, Kageyama D, Stouthamer R (2012) Distribution patterns of Wolbachia endosymbionts in the closely related flower bugs of the genus Orius: implications for coevolution and horizontal transfer. Microb Ecol 64: 537-545.
46. Whitcomb RF, Chen TA, Williamson DL, Liao C, Tully JG, Bové JM, Mouchès C, Rose DL, Coan ME, Clark TB (1986) Spiroplasmakunkelii sp. nov.: characterization of the etiological agent of corn stunt disease. Int J Syst Bacteriol 36: 170-178.
47. Williamson DL, Sakaguchi B, Hackett KJ, Whitcomb RF, Tully JG, Carle P, Bové JM, Adams JR, Konai M, Henegar RB (1999) Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int J Syst Bacteriol 49: 611-618.
48. Yano E (2004) Recent development of biological control and IPM in greenhouses in Japan. J Asia-Pac Entomol 7: 5-11.
49. Yasunaga T (1997) The flower bug genus Orius Wolff (Heteroptera: Anthocoridae) from Japan and Taiwan, part I. Appl Entomol Zool 32: 355-364.
50. Yasunaga T (1997) The flower bug genus Orius Wolff (Heteroptera: Anthocoridae) from Japan and Taiwan, part II. Appl Entomol Zool 32: 379-386.
51. Yasunaga T (1997) The flower bug genus Orius Wolff (Heteroptera: Anthocoridae) from Japan and Taiwan, part III. Appl Entomol Zool 32: 387-394.
52. Kashio T, Yasunaga T (1993) Taxonomy and identification of Japanese Orius species. Plant Prot 47: 180-183 (in Japanese).