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

Applied and Environmental Microbiology

Volumn 75, Issue 21, 2009, Pages 6757-6763

  Nakamura, Yuki ^a,b   Kawai, Sawako ^a   Yukuhiro, Fumiko ^a   Ito, Saiko ^c   Gotoh, Tetsuo ^c   Kisimoto, Ryoiti ^d   Yanase, Tohru ^e   Matsumoto, Yukiko ^a   Kageyama, Daisuke ^a   Noda, Hiroaki ^a,b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c IBARAKI UNIVERSITY   (Japan)

^d National Institute of Animal Health ^*  (Japan)

^e NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; BACTEROIDES; FLAVOBACTERIUM; HIGH FREQUENCY; IN-PLANTS; INTRACELLULAR BACTERIA; MICROFILAMENTS; MOLECULAR DATA; MORPHOLOGICAL FEATURES; SINGLE SPECIES; SPIDER MITE; TAXONOMIC REVISION;

BACTERIOLOGY;

DNA TOPOISOMERASE (ATP HYDROLYSING) B; RNA 16S;

ABNORMALITY; FLY; HOST-PARASITE INTERACTION; INFECTIOUS DISEASE; MICROBIAL ACTIVITY; MITE; NEMATODE; NOMENCLATURE; PLANTHOPPER; REPRODUCTIVE BEHAVIOR; TAXONOMY;

ACARI; ALPHAPROTEOBACTERIA; ARTHROPOD; ARTICLE; BACTEROIDES; BITING MIDGES; CANDIDATUS CARDINIUM HERTIGII; CYTOPHAGA; FEMALE; FLAVOBACTERIUM; FLY; HEMIPTERA; MICROFILAMENT; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANTHOPPER; SPIDER MITE; TAXONOMY; WOLBACHIA;

ANIMALS; ARTHROPODS; BACTERIAL INFECTIONS; BACTEROIDETES; CLUSTER ANALYSIS; DNA GYRASE; DNA, BACTERIAL; DNA, RIBOSOMAL; PHYLOGENY; PREVALENCE; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

ACARI; ALPHAPROTEOBACTERIA; ARANEAE; ARCHAEORRHYNCHA; ARTHROPODA; BACTEROIDES; CANDIDATUS CARDINIUM; CANDIDATUS CARDINIUM HERTIGII; CERATOPOGONIDAE; CYTOPHAGA; FLAVOBACTERIUM; NEMATODA; TETRANYCHIDAE; VESPOIDEA; WOLBACHIA;

EID: 70350520501     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01583-09     Document Type: Article

References (52)

1. Amann, R., C. Lin, R. Key, L. Montgomery, and D. Stahl. 1992. Diversity among Fibrobacter isolates: towards a phylogenetic classification. Syst. Appl. Microbiol. 15:23-31.
2. Bandi, C., T. J. Anderson, C. Genchi, and M. L. Blaxter. 1998. Phylogeny of Wolbachia in filarial nematodes. Proc. Biol. Sci. 265:2407-2413.
3. Bandi, C., G. Damiani, L. Magrassi, A. Grigolo, R. Fani, and L. Sacchi. 1994. Flavobacteria as intracellular symbionts in cockroaches. Proc. Biol. Sci. 257: 43-48.
4. Bandi, C., M. Sironi, G. Damiani, L. Magrassi, C. A. Nalepa, U. Laudani, and L. Sacchi. 1995. The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc. Biol. Sci. 259:293-299.
5. Baumann, P. 2005. Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155-189.
6. Bigliardi, E., L. Sacchi, M. Genchi, A. Alma, M. Pajoro, D. Daffonchio, M. Marzorati, and A. M. Avanzati. 2006. Ultrastructure of a novel Cardinium sp. symbiont in Scaphoideus titanus (Hemiptera: Cicadellidae). Tissue Cell 38: 257-261.
7. Boyle, L., S. L. O'Neill, H. M. Robertson, and T. L. Karr. 1993. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260:1796-1799. (Pubitemid 23244203)
8. Breeuwer, J. A., R. Stouthamer, S. M. Barns, D. A. Pelletier, W. G. Weisburg, and J. H. Werren. 1992. Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol. Biol. 1:25-36.
9. Casiraghi, M., T. J. Anderson, C. Bandi, C. Bazzocchi, and C. Genchi. 2001. A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122:93-103.
10. Dale, C., M. Beeton, C. Harbison, T. Jones, and M. Pontes. 2006. Isolation, pure culture, and characterization of "Candidatus Arsenophonus arthropodicus," an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl. Environ. Microbiol. 72:2997-3004.
11. Duron, O., D. Bouchon, S. Boutin, L. Bellamy, L. Zhou, J. Engelstadter, and G. D. Hurst. 2008. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 6:27.
12. Duron, O., G. D. Hurst, E. A. Hornett, J. A. Josling, and J. Engelstadter. 2008. High incidence of the maternally inherited bacterium Cardinium in spiders. Mol. Ecol. 17:1427-1437.
13. Enigl, M., and P. Schausberger. 2007. Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Exp. Appl. Acarol. 42:75-85.
14. Gotoh, T., H. Noda, and S. Ito. 2007. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13-20.
15. Groot, T. V., and J. A. Breeuwer. 2006. Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Exp. Appl. Acarol. 39:257-271.
16. Hilgenboecker, K., P. Hammerstein, P. Schlattmann, A. Telschow, and J. H. Werren. 2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. 281:215-220.
17. Horn, M., M. D. Harzenetter, T. Linner, E. N. Schmid, K. D. Muller, R. Michel, and M. Wagner. 2001. Members of the Cytophaga-Flavobacterium- Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus.' Environ. Microbiol. 3:440-449.
18. Hotopp, J. C., M. E. Clark, D. C. Oliveira, J. M. Foster, P. Fischer, M. C. Torres, J. D. Giebel, N. Kumar, N. Ishmael, S. Wang, J. Ingram, R. V. Nene, J. Shepard, J. Tomkins, S. Richards, D. J. Spiro, E. Ghedin, B. E. Slatko, H. Tettelin, and J. H. Werren. 2007. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753-1756. (Pubitemid 47461840)
19. Hoy, M. A., and A. Jeyaprakash. 2005. Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biol. Control 32:427-441.
20. Hunter, M. S., S. J. Perlman, and S. E. Kelly. 2003. A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc. Biol. Sci. 270:2185-2190.
21. Hurst, G. D. D., T. C. Hammarton, C. Bandi, T. M. O. Majerus, D. Bertrand, and M. E. N. Majerus. 1997. The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet. Res. 70:1-6.
22. Kurtti, T. J., U. G. Munderloh, T. G. Andreadis, L. A. Magnarelli, and T. N. Mather. 1996. Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis. J. Invertebr. Pathol. 67:318-321. (Pubitemid 126315921)
23. Lo, N., C. Paraskevopoulos, K. Bourtzis, S. L. O'Neill, J. H. Werren, S. R. Bordenstein, and C. Bandi. 2007. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int. J. Syst. Evol. Microbiol. 57:654-657.
24. Marzorati, M., A. Alma, L. Sacchi, M. Pajoro, S. Palermo, L. Brusetti, N. Raddadi, A. Balloi, R. Tedeschi, E. Clementi, S. Corona, F. Quaglino, P. A. Bianco, T. Beninati, C. Bandi, and D. Daffonchio. 2006. A novel Bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of Flavescence doree in Vitis vinifera. Appl. Environ. Microbiol. 72:1467-1475. (Pubitemid 43271261)
25. Matalon, Y., N. Katzir, Y. Gottlieb, V. Portnoy, and E. Zchori-Fein. 2007. Cardinium in Plagiomerus diaspidis (Hymenoptera: Encyrtidae). J. Invertebr. Pathol. 96:106-108.
26. Matsumoto, Y., T. Yanase, T. Tsuda, and H. Noda. 2009. Species-specific mitochondrial gene rearrangements in biting midges and vector species identification. Med. Vet. Entomol. 23:47-55.
27. Mellor, P. S., J. Boorman, and M. Baylis. 2000. Culicoides biting midges: their role as arbovirus vectors. Annu. Rev. Entomol. 45:307-340.
28. Morimoto, S., T. J. Kurtti, and H. Noda. 2006. In vitro cultivation and antibiotic susceptibility of a Cytophaga-like intracellular symbiote isolated from the tick Ixodes scapularis. Curr. Microbiol. 52:324-329.
29. Navajas, M., J. Gutierrez, O. Bonato, H. R. Bolland, and S. Mapangou- Divassa. 1994. Intraspecific diversity of the Cassava green mite Mononychellus progresivus (Acari: Tetranychidae) using comparisons of mitochondrial and nuclear ribosomal DNA sequences and cross-breeding. Exp. Appl. Acarol. 18:351-360.
30. Nei, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York, NY.
31. Noel, G. R., and N. Atibalentja. 2006. 'Candidatus Paenicardinium endonii,' an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. Int. J. Syst. Evol. Microbiol. 56:1697-1702.
32. O'Neill, S. L., R. Giordano, A. M. Colbert, T. L. Karr, and H. M. Robertson. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. USA 89:2699-2702.
33. Pfarr, K., J. Foster, B. Slatko, A. Hoerauf, and J. A. Eisen. 2007. On the taxonomic status of the intracellular bacterium Wolbachia pipientis: should this species name include the intracellular bacteria of filarial nematodes? Int. J. Syst. Evol. Microbiol. 57:1677-1678.
34. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. (Pubitemid 28552116)
35. Ros, V. I., and J. A. Breeuwer. 2009. The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102:413-422.
36. Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497. (Pubitemid 38016658)
37. Sacchi, L., M. Genchi, E. Clementi, E. Bigliardi, A. M. Avanzati, M. Pajoro, I. Negri, M. Marzorati, E. Gonella, A. Alma, D. Daffonchio, and C. Bandi. 2008. Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue Cell 40:231-242.
38. Sheoheherd, A. M., S. A. Clark, and A. Kempton. 1973. An intracellular micro-organism associated with tissues of Heterodera spp. Nematologica 19:31-34.
39. Stackebrandt, E., and B. M. Goebel. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-849.
40. Stouthamer, R., J. A. Breeuwert, R. F. Luck, and J. H. Werren. 1993. Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66-68. (Pubitemid 23020774)
41. Suzuki, M., Y. Nakagawa, S. Harayama, and S. Yamamoto. 1999. Phylogenetic analysis of genus Marinilabilia and related bacteria based on the amino acid sequences of GyrB and emended description of Marinilabilia salmonicolor with Marinilabilia agarovorans as its subjective synonym. Int. J. Syst. Bacteriol. 49:1551-1557.
42. Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sinauer Associates, Inc., Sunderland, MA.
43. Tajima, F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460. (Pubitemid 14247444)
44. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL-X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
45. Weeks, A. R., F. Marec, and J. A. Breeuwer. 2001. A mite species that consists entirely of haploid females. Science 292:2479-2482.
46. Weeks, A. R., R. Velten, and R. Stouthamer. 2003. Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc. Biol. Sci. 270:1857-1865.
47. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
48. Werren, J. H., L. Baldo, and M. E. Clark. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6:741-751.
49. Wolfgang, A., R. Markus, N. A. Dimitrios, and S. Christian. 2009. Evidence for low-titre infections in insect symbiosis: Wolbachia in the bark beetle Pityogenes chalcographus (Coleoptera, Scolytinae). Environ. Microbiol. 11: 1923-1933.
50. Zchori-Fein, E., Y. Gottlieb, S. E. Kelly, J. K. Brown, J. M. Wilson, T. L. Karr, and M. S. Hunter. 2001. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc. Natl. Acad. Sci. USA 98:12555-12560.
51. Zchori-Fein, E., and S. J. Perlman. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13:2009-2016.
52. Zchori-Fein, E., S. J. Perlman, S. E. Kelly, N. Katzir, and M. S. Hunter. 2004. Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii.' Int. J. Syst. Evol. Microbiol. 54:961-968. (Pubitemid 38771803)