Tissue tropism and vertical transmission of Coxiella in Rhipicephalus sanguineus and Rhipicephalus turanicus ticks

Environmental Microbiology

Volumn 16, Issue 12, 2014, Pages 3657-3668

  Lalzar, Itai ^a   Friedmann, Yael ^a   Gottlieb, Yuval ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPODA; COXIELLA; IXODIDA; RHIPICEPHALUS SANGUINEUS; RHIPICEPHALUS TURANICUS; RICKETTSIA;

ANIMAL; BACTERIAL LOAD; COXIELLA; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GONAD; GROWTH, DEVELOPMENT AND AGING; MALE; MALPIGHIAN TUBULE; MICROBIOLOGY; OOCYTE; PHYSIOLOGY; RHIPICEPHALUS; RHIPICEPHALUS SANGUINEUS; RICKETTSIA; SYMBIOSIS;

ANIMALS; BACTERIAL LOAD; COXIELLA; FEMALE; GONADS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MALPIGHIAN TUBULES; OOCYTES; RHIPICEPHALUS; RHIPICEPHALUS SANGUINEUS; RICKETTSIA; SYMBIOSIS;

EID: 84921607690     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12455     Document Type: Article

References (56)

1. Almeida, A.P., Marcili, A., Leite, R.C., Nieri-Bastos, F.A., Domingues, L.N., Martins, J.R., and Labruna, M.B. (2012) Coxiella symbiont in the tick Ornithodoros rostratus (Acari: Argasidae). Ticks Tick Borne Dis 3: 203-206.
2. Balashov, Y.S. (1972) Bloodsucking Ticks (Ixodoidea) - Vectors of Diseases of Man and Animals. Annapolis, MD, USA: Entomological Society of America.
3. Balashov, Y.S. (1983) An Atlas of Ixodid Tick Ultrastructure. Annapolis, MD, USA: Entomological Society of America.
4. Balmand, S., Lohs, C., Aksoy, S., and Heddi, A. (2013) Tissue distribution and transmission routes for the tsetse fly endosymbionts. J Invertebr Pathol 112: S116-S122.
5. Bian, G., Joshi, D., Dong, Y., Lu, P., Zhou, G., Pan, X., etal. (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340: 748-751.
6. van Borm, S., Buschinger, A., Boomsma, J.J., and Billen, J. (2002) Tetraponera ants have gut symbionts related to nitrogen-fixing root-nodule bacteria. Proc Biol Sci 269: 2023-2027.
7. Brumin, M., Levy, M., and Ghanim, M. (2012) Transovarial transmission of Rickettsia spp. and organ-specific infection of the whitefly Bemisia tabaci. Appl Environ Microbiol 78: 5565-5574.
8. Burgdorfer, W., Hayes, S.F., and Mavros, A.J. (1981) Nonpathogenic Rickettsiae in Dermacentor andersoni: a limiting factor for the distribution of Rickettsia Rickettsii. In Rickettsiae and Rickettsial Diseases. Burgdorfer, W., and Anacker, R.L. (eds). New York, USA: Academic Press, pp. 585-594.
9. Clancy, D.J., and Hoffmann, A.A. (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol Exp Appl 86: 13-24.
10. Dantas-Torres, F., Latrofa, M.S., Annoscia, G., Giannelli, A., Parisi, A., and Otranto, D. (2013) Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasite Vector 6: 213.
11. Dobson, S.L., Bourtzis, K., Braig, H.R., Jones, B.F., Zhou, W.G., Rousset, F., and O'Neill, S.L. (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 29: 153-160.
12. Edwards, K.T., Goddard, J., and Varela-Stokes, A.S. (2009) Examination of the internal morphology of the ixodid tick, Amblyomma maculatum Koch (Acari: Ixodidae); a 'how-to' pictorial dissection guide. Midsouth Entomol 2: 28-39.
13. Flannagan, R.S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
14. Frentiu, F.D., Robinson, J., Young, P.R., McGraw, E.A., and O'Neill, S.L. (2010) Wolbachia mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE 5: e13398.
15. Frydman, H.M., Li, J.M., Robson, D.N., and Wieschaus, E. (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441: 509-512.
16. de la Fuente, J., Estrada-Pena, A., Venzal, J.M., Kocan, K.M., and Sonenshine, D.E. (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13: 6938-6946.
17. Ghanim, M., and Kontsedalov, S. (2009) Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag Sci 65: 939-942.
18. Goto, S., Anbutsu, H., and Fukatsu, T. (2006) Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl Environ Microbiol 72: 4805-4810.
19. Hajdusek, O., Sojka, D., Kopacek, P., Buresova, V., Franta, Z., Sauman, I., etal. (2009) Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proc Natl Acad Sci USA 106: 1033-1038.
20. Herren, J.K., Paredes, J.C., Schüpfer, F., and Lemaitre, B. (2013) Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. mBio. 4: e00532-12.
21. Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.-Y., and Fukatsu, T. (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107: 769-774.
22. Klyachko, O., Stein, B.D., Grindle, N., Clay, K., and Fuqua, C. (2007) Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl Environ Microbiol 73: 6584-6594.
23. Koga, R., Meng, X.-Y., Tsuchida, T., and Fukatsu, T. (2012) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte - embryo interface. Proc Natl Acad Sci USA 109: E1230-E1237.
24. Kölsch, G., and Pedersen, B.V. (2010) Can the tight co-speciation between reed beetles (Col., Chrysomelidae, Donaciinae) and their bacterial endosymbionts, which provide cocoon material, clarify the deeper phylogeny of the hosts? Mol Phylogenet Evol 54: 810-821.
25. Kuechler, S.M., Gibbs, G., Burckhardt, D., Dettner, K., and Hartung, V. (2013) Diversity of bacterial endosymbionts and bacteria - host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). Environ Microbiol 15: 2031-2042.
26. Lalzar, I., Harrus, S., Mumcuoglu, K.Y., and Gottlieb, Y. (2012) Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl Environ Microbiol 78: 4110-4116.
27. Lewis, D. (1979) Detection of Rickettsia-like microorganisms within the ovaries of female Ixodes ricinus ticks. Z Parasitol Res 59: 295-298.
28. Li, T., Xiao, J.-H., Xu, Z.-H., Murphy, R.W., and Huang, D.-W. (2011) Cellular tropism, population dynamics, host range and taxonomic status of an aphid secondary symbiont, SMLS (Sitobion miscanthi L type symbiont). PLoS ONE 6: e21944.
29. Lopez-Sanchez, M.J., Neef, A., Pereto, J., Patino-Navarrete, R., Pignatelli, M., Latorre, A., and Moya, A. (2009) Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet 5: e1000721.
30. Macaluso, K.R., Sonenshine, D.E., Ceraul, S.M., and Azad, A.F. (2002) Rickettsial infection in Dermacentor variabilis (Acari: Ixodidae) inhibits transovarial transmission of a second Rickettsia. J Med Entomol 39: 809-813.
31. Machado-Ferreira, E., Dietrich, G., Hojgaard, A., Levin, M., Piesman, J., Zeidner, N.S., and Soares, C.A.G. (2011) Coxiella symbionts in the Cayenne tick Amblyomma cajennense. Microb Ecol 62: 134-142.
32. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K.H. (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria - problems and solutions. Syst Appl Microbiol 15: 593-600.
33. Matsumoto, K., Ogawa, M., Brouqui, P., Raoult, D., and Parola, P. (2005) Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol 19: 263-270.
34. Min, K.-T., and Benzer, S. (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 94: 10792-10796.
35. Moran, N.A., McCutcheon, J.P., and Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
36. Mudrow, E. (1932) Über die intrazellulären symbionten der zecken. Z Parasitenkd 5: 138-183.
37. Niebylski, M.L., Schrumpf, M.E., Burgdorfer, W., Fischer, E.R., Gage, K.L., and Schwan, T.G. (1997) Rickettsia peacockii sp. nov., a new species infecting wood ticks, Dermacentor andersoni, in western Montana. Int J Syst Bacteriol 47: 446-452.
38. Noda, H., Munderloh, U.G., and Kurtti, T.J. (1997) Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol 63: 3926-3932.
39. Osborne, S.E., Iturbe-Ormaetxe, I., Brownlie, J.C., O'Neill, S.L., and Johnson, K.N. (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 78: 6922-6929.
40. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
41. Sabree, Z.L., Kambhampati, S., and Moran, N.A. (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci USA 106: 19521-19526.
42. Sakurai, M., Koga, R., Tsuchida, T., Meng, X.Y., and Fukatsu, T. (2005) Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera. Appl Environ Microbiol 71: 4069-4075.
43. van Schaik, E.J., Chen, C., Mertens, K., Weber, M.M., and Samuel, J.E. (2013) Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nat Rev Microbiol 11: 561-573.
44. Serbus, L.R., Casper-Lindley, C., Landmann, F., and Sullivan, W. (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42: 683-707.
45. da Silva Costa, L., Nunes, P., Soares, J., Labruna, M., and Camargo-Mathias, M. (2011) Distribution of Rickettsia rickettsii in ovary cells of Rhipicephalus sanguineus (Latreille 1806) (Acari: Ixodidae). Parasite Vector 4: 222.
46. Snyder, A.K., Deberry, J.W., Runyen-Janecky, L., and Rio, R.V.M. (2010) Nutrient provisioning facilitates homeostasis between tsetse fly (Diptera: Glossinidae) symbionts. Proc R Soc B 277: 2389-2397.
47. Socolovschi, C., Mediannikov, O., Raoult, D., and Parola, P. (2009) The relationship between spotted fever group Rickettsiae and Ixodid ticks. Vet Res 40: 34.
48. Sonenshine, D.E. (1991) Biology of Ticks. New York, USA: Oxford University Press.
49. Strunov, A., Kiseleva, E., and Gottlieb, Y. (2013) Spatial and temporal distribution of pathogenic Wolbachia strain wMelPop in Drosophila melanogaster central nervous system under different temperature conditions. J Invertebr Pathol 114: 22-30.
50. Taylor, M., Mediannikov, O., Raoult, D., and Greub, G. (2012) Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol Med Microbiol 64: 21-31.
51. Toomey, M.E., Panaram, K., Fast, E.M., Beatty, C., and Frydman, H.M. (2013) Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection. Proc Natl Acad Sci USA 110: 10788-10793.
52. Walker, J.B., Keirans, J.E., and Horak, I.G. (2000) The Genus Rhipicephalus (Acari: Ixodidae): A Guide to the Brown Ticks of the World. New York, USA: Cambridge University Press.
53. Walker, T., Johnson, P.H., Moreira, L.A., Iturbe-Ormaetxe, I., Frentiu, F.D., McMeniman, C.J., etal. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450-453.
54. Zchori-Fein, E., Gottlieb, Y., and Coll, M. (2000) Wolbachia density and host fitness components in Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J Invertebr Pathol 75: 267-272.
55. Zhong, J., Jasinskas, A., and Barbour, A.G. (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS ONE 2: e405.
56. Zindel, R., Gottlieb, Y., and Aebi, A. (2011) Arthropod symbioses: a neglected parameter in pest- and disease-control programmes. J Appl Ecol 48: 864-872.