Advertisement

Folia Microbiologica

, Volume 58, Issue 5, pp 419–428 | Cite as

Hard ticks and their bacterial endosymbionts (or would be pathogens)

  • Arunee Ahantarig
  • Wachareeporn Trinachartvanit
  • Visut Baimai
  • Libor Grubhoffer
Article

Abstract

The symbiotic microorganisms of arthropod vectors are highly significant from several points of view, partly due to their possible roles in the transmission of pathogenic causative agents by blood-sucking vectors. Although ticks are well studied because of their significance to human health, novel microbial associations remain to be described. This review summarises several endosymbiotic bacterial species in hard ticks from various parts of the world, including Coxiella-, Francisella-, Rickettsia- and Arsenophonus-like symbionts as well as Candidatus Midichloria mitochondrii and Wolbachia. New methodologies for the isolation and characterization of tick-associated bacteria will, in turn, encourage new strategies of tick control by studying their endosymbionts.

Keywords

Tick Species Bacterial Symbiont Spotted Fever Tularemia Tick Control 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by Mahidol University Research grant SCJV1099000737 and the Faculty of Science, Mahidol University, Thailand research grant, SCM55-004. The authors thank Professor Sansanee Chaiyaroj from the Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, Thailand for her advice and support in the research areas of ticks and tick-borne diseases.

References

  1. Ahantarig A, Kittayapong P (2011) Endosymbiotic Wolbachia bacteria as biological control tools of disease vectors and pests. J Appl Entomol 135:479–486CrossRefGoogle Scholar
  2. Ahantarig A, Malaisri P, Hirunkanokpun S, Sumrandee C, Trinachartvanit W, Baimai V (2011) Detection of Rickettsia and a novel Haemaphysalis shimoga symbiont bacterium in ticks in Thailand. Curr Microbiol 62:1502–1502. doi: 10.1007/s00284-011-9887-3 Google Scholar
  3. Andreotti R, Pérez de León AA, Dowd SE, Guerrero FD, Bendele KG, Scoles GA (2011) Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) through tag- encoded pyrosequencing. BMC Microbiol 6:11(1):6Google Scholar
  4. Apperson CS, Engber B, Nicholson WL, Mead DG, Engel J, Yabsley MJ, Dail K, Johnson J, Watson DW (2008) Tick-borne diseases in North Carolina: is "Rickettsia amblyommii" a possible cause of rickettsiosis reported as Rocky Mountain spotted fever? Vector Borne Zoonotic Dis 8:597–606CrossRefPubMedGoogle Scholar
  5. Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis 4:179–186CrossRefPubMedGoogle Scholar
  6. Baimai V (2010) Why do we need basic research? Bangkok Printing, BangkokGoogle Scholar
  7. Baldo L, Prendini L, Corthals A, Werren JH (2007) Wolbachia are present in southern African scorpions and cluster with supergroup F. Curr Microbiol 55:367–373CrossRefPubMedGoogle Scholar
  8. Baldridge GD, Burkhardt NY, Simser JA, Kurtti TJ, Munderloh UG (2004) Sequence and expression analysis of the ompA gene of Rickettsia peacockii, an endosymbiont of the Rocky Mountain wood tick, Dermacentor andersoni. Appl Environ Microbiol 70:6628–6636CrossRefPubMedGoogle Scholar
  9. Bell JE, Kohls GM, Stoenner HG, Blackman DB (1963) Non-pathogenic rickettsias related to the spotted fever group from ticks, Dermacentor variabilis and Dermacentor andersoni from eastern Montana. J Immunol 90:770–781PubMedGoogle Scholar
  10. Beninati T, Lo N, Sacchi L, Genchi C, Noda H, Bandi C (2004) A novel alpha-Proteobacterium resides in the mitochondria of ovarian cells of the tick Ixodes ricinus. Appl Environ Microbiol 70:2596–2602CrossRefPubMedGoogle Scholar
  11. Benson MJ, Gawronski JD, Eveleigh DE, Benson DR (2004) Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol 70:616–620CrossRefPubMedGoogle Scholar
  12. Bernasconi MV, Casati S, Péter O, Piffaretti JC (2002) Rhipicephalus ticks infected with Rickettsia and Coxiella in Southern Switzerland (Canton Ticino). Infect Genet Evol 2:111–120CrossRefPubMedGoogle Scholar
  13. Broadwater AH, Sonenshine DE, Hynes WL, Ceraul S, De SA (2002) Glass capillary tube feeding: a method for infecting nymphal Ixodes scapularis (Acari: Ixodidae) with the Lyme disease spirochete Borrelia burgdorferi. J Med Entomol 39:285–292CrossRefPubMedGoogle Scholar
  14. Brouqui P, Dupont HT, Drancourt M, Berland Y, Etienne J, Leport C, Goldstein F, Massip P, Micoud M, Bertrand A et al (1993) Chronic Q fever. Ninety-two cases from France, including 27 cases without endocarditis. Arch Intern Med 153:642–648CrossRefPubMedGoogle Scholar
  15. Burgdorfer W (1988) Ecological and epidemiological considerations of Rocky Mountain spotted fever and scrub typhus. In: Walker DH (ed) Biology of rickettsial diseases. CRC Press, Boca Raton, pp 33–50Google Scholar
  16. Burgdorfer W, Brinton LP, Hughes LE (1973) Isolation and characterization of symbiotes from the Rocky Mountain wood tick Dermacentor andersoni. J Invertebr Pathol 22:424–434CrossRefPubMedGoogle Scholar
  17. Burgdorfer W, Hayes SF, Mavros AJ (1981) Non-Pathogenic Rickettsiae in Dermacentor andersoni: A Limiting Factor for the Distribution of Rickettsia rickettsii. In: Burgdorfer W, Anacker RL (eds) Rickettsiae and Rickettsial Disease. Academic, New York, pp 585–594Google Scholar
  18. Carmichael JR, Fuerst PA (2006) A rickettsial mixed infection in a Dermacentor variabilis tick from Ohio. Ann N Y Acad Sci 1078:334–337CrossRefPubMedGoogle Scholar
  19. Childs JE, Paddock CD (2002) Passive surveillance as an instrument to identify risk factors for fatal Rocky Mountain spotted fever: is there more to learn? AmJTrop Med Hyg 66:450–457Google Scholar
  20. Clay K, Fuqua C, Lively C, Wade M (2006) Microbial community ecology of tick-borne human pathogens. In: Collinge S, Ray C (eds) Disease Ecology. University Press, Oxford, pp 41–57Google Scholar
  21. Clay K, Klyachko O, Grindle N, Civitello D, Oleske D, Fuqua C (2008) Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol Ecol 17:4371–4381CrossRefPubMedGoogle Scholar
  22. Cotte V, Bonnet S, Cote M, Vayssier-Taussat M (2010) Prevalence of five pathogenic agents in questing Ixodes ricinus ticks from western France. Vector Borne Zoonotic Dis 10:723–730CrossRefPubMedGoogle Scholar
  23. Cowdry EV (1925) A group of micro-organisms transmitted hereditarily in ticks and apparently unassociated with disease. J Exp Med 41:817–830CrossRefPubMedGoogle Scholar
  24. Dale C, Beeton M, Harbison C, Jones T, Pontes M (2006) Isolation, pure culture, and characterization of ‘Candidatus Arsenophonus arthropodicus’, an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72:2997–3004CrossRefPubMedGoogle Scholar
  25. de la Fuente J, Blouin EF, Kocan KM (2003) Infection exclusion of the rickettsial pathogen Anaplasma marginale in the tick vector Dermacentor variabilis. Clin Diagn Lab Immunol 10:182–184PubMedGoogle Scholar
  26. Dergousoff SJ, Chilton NB (2010) Detection of a new Arsenophonus-type bacterium in Canadian populations of the Rocky Mountain wood tick, Dermacentor andersoni. Exp Appl Acarol 52:85–91CrossRefPubMedGoogle Scholar
  27. Epis S, Sassera D, Beninati T, Lo N, Beati L, Piesman J, Rinaldi L, McCoy KD, Torina A, Sacchi L, Clementi E, Genchi M, Magnino S, Bandi C (2008) Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology 135:485–494CrossRefPubMedGoogle Scholar
  28. Fujita O, Tatsumi M, Tanabayashi K, Yamada A (2006) Development of a real-time PCR assay for detection and quantification of Francisella tularensis. Jpn J Infect Dis 59:46–51PubMedGoogle Scholar
  29. Gage KL, Schrumpf ME, Karstens RH, Burgdorfer W, Schwan TG (1994) DNA typing of rickettsiae in naturally infected ticks using a polymerase chain reaction/restriction fragment length polymorphism system. AmJTrop Med Hyg 50:247–260Google Scholar
  30. Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, Brenner DJ (1991) Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic was Nasonia vitripennis. Int J Syst Bacteriol 41:563–568CrossRefGoogle Scholar
  31. Gillespie JJ, Joardar V, Williams KP, Driscoll T, Hostetler JB, Nordberg E, Shukla M, Walenz B, Hill CA, Nene VM, Azad AF, Sobral BW, Caler E (2011) A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. J Bacteriol 94:376–394Google Scholar
  32. Goddard J (2009) Historical and recent evidence for close relationships among Rickettsia parkeri, R. conorii, R. africae, and R. sibirica: implications for rickettsial taxonomy. J Vector Ecol 34:238–242PubMedGoogle Scholar
  33. Grindle N, Tyner JJ, Clay K, Fuqua C (2003) Identification of Arsenophonus-type bacteria from the dog tick Dermacentor variabilis. J Invertebr Pathol 83:264–266CrossRefPubMedGoogle Scholar
  34. Halos L, Bord S, Cotté V, Gasqui P, Abrial D, Barnouin J, Boulouis HJ, Vayssier-Taussat M, Vourc'h G (2010) Ecological factors characterizing the prevalence of bacterial tick-borne pathogensin Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol 76:4413–4420CrossRefPubMedGoogle Scholar
  35. Harden VA (1990) Rocky Mountain spotted fever: history of a twentieth century disease. The Johns Hopkins University Press. Baltimore, MarylandGoogle Scholar
  36. Harrus S, Perlman-Avrahami A, Mumcuoglu KY, Morick D, Eyal O, Baneth G (2011) Molecular detection of Ehrlichia canis, Anaplasma bovis, Anaplasma platys, Candidatus Midichloria mitochondrii and Babesia canis vogeli in ticks from Israel. Clin Microbiol Infect 17:459–463CrossRefPubMedGoogle Scholar
  37. Hartelt K, Oehme R, Frank H, Brockmann SO, Hassler D, Kimmig P (2004) Pathogens and symbionts in ticks: prevalence of Anaplasma phagocytophilum (Ehrlichia sp.), Wolbachia sp., Rickettsia sp., and Babesia sp. in Southern Germany. Int J Med Microbiol 293(Suppl 37):86–92PubMedGoogle Scholar
  38. Hayes SF, Burgdorfer W (1981) Ultrastructural comparisons of Wolbachia-like symbiote of ticks (Acari: Ixodidae). In: Burgdorfer W, Anacker AL (eds) Rickettsiae and Rickettsial Diseases. Academic Press, New York, pp 281–333Google Scholar
  39. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia? - a statistical analysis of current data. FEMS Microbiol Lett 281:215–220CrossRefPubMedGoogle Scholar
  40. Hirunkanokpun S, Kittayapong P, Cornet JP, Gonzalez JP (2003) Molecular evidence for novel tick-associated spotted fever group rickettsiae from Thailand. J Med Entomol 40:230–237Google Scholar
  41. Inokuma H, Raoult D, Brouqui P (2000) Detection of Ehrlichia platys DNA in brown dog ticks (Rhipicephalus sanguineus) in Okinawa Island, Japan. J Clin Microbiol 38:4219–4221PubMedGoogle Scholar
  42. Jasinskas A, Zhong J, Barbour AG (2007) Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl Environ Microbiol 73:334–336CrossRefPubMedGoogle Scholar
  43. Jellison WL (1974) Tularemia in North America, 1930–1974. University of Montana, MissoulaGoogle Scholar
  44. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129:S3–S14CrossRefPubMedGoogle Scholar
  45. Klyachko O, Stein B, Grindle N, Clay K, Fuqua C (2007) Localization and visualization of a Coxiella-type symbiont within the Lone Star Tick Amblyomma americanum. Appl Environ Microbiol 73:6584–6594CrossRefPubMedGoogle Scholar
  46. Kollars TM Jr, Tippayachai B, Bodhidatta D (2001) Short report: Thai tick typhus, Rickettsia honei, and a unique rickettsia detected in Ixodes granulatus (Ixodidae: Acari) from Thailand. AmJTrop Med Hyg 65:535–537Google Scholar
  47. Kurtti TJ, Palmer AT, Oliver JH Jr (2002) Rickettsia-like bacteria in Ixodes woodi (Acari: Ixodidae). J Med Entomol 39:534–540CrossRefPubMedGoogle Scholar
  48. Lee JH, Park HS, Jang WJ, Koh SE, Park TK, Kang SS, Kim BJ, Kook YH, Park KH, Lee SH (2004) Identification of the Coxiella sp detected from Haemaphysalis longicornis ticks in Korea. Micro Immun 48:125–130Google Scholar
  49. Lewis D (1979) The detection of rickettsia-like microorganisms within the ovaries of female Ixodes ricinus ticks. Z Parasitenkd 59:295–298CrossRefPubMedGoogle Scholar
  50. Lively CM, Clay K, Wade WJ, Fuqua C (2005) Competitive coexistence of vertically and horizontally transmitted parasites. Evol Ecol Res 7:1183–1190Google Scholar
  51. Lo N, Beninati T, Sassera D, Bouman EA, Santagati S, Gern L, Sambri V, Masuzawa T, Gray JS, Jaenson TG, Bouattour A, Kenny MJ, Guner ES, Kharitonenkov IG, Bitam I, Bandi C (2006) Widespread distribution and high prevalence of an alpha proteobacterial symbiont in the tick Ixodes ricinus. Environ Microbiol 8:1280–1287CrossRefPubMedGoogle Scholar
  52. Macaluso KR, Sonenshine DE, Ceraul SM, Azad AF (2002) Rickettsial infection in Dermocentor variabilis (Acari: Ixodidae) inhibits transovarial transmission of a second Rickettsia. J Med Entomol 39:809–813CrossRefPubMedGoogle Scholar
  53. Magnarelli LA, Anderson JF, Burgdorfer W, Philip RN, Chappell WA (1985) Spotted fever group rickettsiae in immature and adult ticks (Acari: Ixodidae) from a focus of Rocky Mountain spotted fever in Connecticut. Can J Microbiol 12:1131–1135CrossRefGoogle Scholar
  54. Mediannikov O, Ivanov L, Nishikawa M, Saito R, Sidelnikov YN, Zdanovskaya NI, Tarasevich IV, Suzuki H (2003) Molecular evidence of Coxiella-like microorganism harbored by Haemaphysalis concinnae ticks in the Russian Far East. Ann N Y Acad Sci 990:226–228CrossRefPubMedGoogle Scholar
  55. Mixson TR, Campbell SR, Gill JS, Ginsberg HS, Reichard MV, Schulze TL, Dasch GA (2006) Prevalence of Ehrlichia, Borrelia, and Rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine states. J Med Entomol 43:1261–1268CrossRefPubMedGoogle Scholar
  56. Morimoto S, Kurtti TJ, Noda H (2006) In vitro cultivation and antibiotic susceptibility of a Cytophaga-like intracellular symbiote isolated from the tick Ixodes scapularis. Current Microbiol 52:324–329CrossRefPubMedGoogle Scholar
  57. Mudrow M (1932) Uber die intrazellularen Symbionten der Zecken. Z Parasitenk 5:138–183CrossRefGoogle Scholar
  58. Munderloh UG, Kurtti TJ (1995) Cellular and molecular interrelationships between ticks and prokaryotic tick borne pathogens. Annu Rev Entomol 40:221–243CrossRefPubMedGoogle Scholar
  59. Munderloh UG, Jauron SD, Kurtti TJ (2005) The tick: a different kind of host for human pathogens. In: Goodman JL, Dennis D, Sonenshine DE (eds) Tick-borne diseases of humans. ASM Press, Washington DC, pp 37–64Google Scholar
  60. Murray RG, Schleifer KH (1994) Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. Int J Syst Bacteriol 44(1):174–176CrossRefPubMedGoogle Scholar
  61. Niebylski ML, Peacock MG, Fischer ER, Porcella SF, Schwan TG (1997a) Characterization of an endosymbiont infecting wood ticks, Dermacentor andersoni, as a member of the genus Francisella. Appl Environ Microbiol 63:3933–3940PubMedGoogle Scholar
  62. Niebylski ML, Schrumpf ME, Burgdorfer W, Fischer ER, Gage KL, Schwan TG (1997b) Rickettsia peacockii sp. nov., a new species infecting wood ticks, Dermacentor andersoni, in Western Montana. Int J Sys Bacteriol 47:446–452CrossRefGoogle Scholar
  63. Niebylski ML, Peacock MG, Schwan TG (1999) Lethal effect of Rickettsia ricketsii on its tick vector (Dermacentor andersoni). Appl Environ Microbiol 65:773–778PubMedGoogle Scholar
  64. Noda H, Munderloh UG, Kurtti TJ (1997) Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol 63:3926–3932PubMedGoogle Scholar
  65. Nováková E, Hypsa V, Moran NA (2009) Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9:143CrossRefPubMedGoogle Scholar
  66. Parola P, Raoult D (2001) Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32:897–928CrossRefPubMedGoogle Scholar
  67. Parola P, Miller RS, McDaniel P, Telford SR 3rd, Rolain JM, Wongsrichanalai C, Raoult D (2003) Emerging rickettsioses of the Thai-Myanmar border. Emerg Infect Dis 9:592–595CrossRefPubMedGoogle Scholar
  68. Peacock MG, Philip RN, Williams JC, Faulkner RS (1983) Serological evaluation of Q fever in humans: enhanced phase I titers of Immunoglobulins G and A are diagnostic for Q fever endocarditis. Infect Immun 41:1089–1098PubMedGoogle Scholar
  69. Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc R Soc Lond B Biol Sci 273:2097–2106CrossRefGoogle Scholar
  70. Perotti MA, Clarke HK, Turner BD, Braig HR (2006) Rickettsia as obligate and mycetomic bacteria. FASEB J 20:2372–2374CrossRefPubMedGoogle Scholar
  71. Philip RN, Casper EA (1981) Serotypes of spotted fever group rickettsiae isolated from Dermacentor andersoni (Stiles) ticks in western Montana. AmJTrop Med Hyg 30:230–238Google Scholar
  72. Plantard O, Bouju-Albert A, Malard MA, Hermouet A, Capron G, Verheyden H (2012) Detection of Wolbachia in the tick Ixodes ricinus is due to the presence of the hymenoptera endoparasitoid Ixodiphagus hookeri. PLoSOne 7:e30692Google Scholar
  73. Raoult D, Roux V (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev 10:694–719PubMedGoogle Scholar
  74. Reis C, Cote M, Paul RE, Bonnet S (2011) Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis 11:907–916CrossRefPubMedGoogle Scholar
  75. Roshdy MA (1968) A rickettsialike (sic) microorganism in the tick Ornithodoros savignyi; observations on its structure and distribution in the tissues of the tick. J Invert Path 11:155–169CrossRefGoogle Scholar
  76. Rowley SM, Raven RJ, McGraw EA (2004) Wolbachia pipientis in Australian spiders. Curr Microbiol 49:208–214CrossRefPubMedGoogle Scholar
  77. Sacchi L, Bigliardi E, Corona S, Beninati T, Lo N, Franceschi A (2004) A symbiont of the tick Ixodes ricinus invades and consumes mitochondria in a mode similar to that of the parasitic bacterium Bdellovibrio bacteriovorus. Tissue Cell 36:43–53Google Scholar
  78. Sanchez JL, Candler WH, Fishbein DB, Greene CR, Coté TR, Kelly DJ, Driggers DP, Johnson BJ (1992) A cluster of tick–borne infections: association with military training and asymptomatic infections due to Rickettsia rickettsii. Trans R Soc Trop Med Hyg 86:321–325CrossRefPubMedGoogle Scholar
  79. Sassera D, Beninati T, Bandi C, Bouman EA, Sacchi L, Fabbi M, Lo N (2006) ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Sys Evol Microbiol 56:2535–2540CrossRefGoogle Scholar
  80. Satta G, Chisu V, Cabras P, Fois F, Masala G (2011) Pathogens and symbionts in ticks:a survey on tick species distribution and presence of tick-transmitted micro-organisms in Sardinia, Italy. J Med Microbiol 60(Pt 1):63–68CrossRefPubMedGoogle Scholar
  81. Schouls LM, van De Pol I, Rijpkema GT, Schot CS (1999) Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol 37:2215–2222PubMedGoogle Scholar
  82. Scoles G (2004) Phylogenetic analysis of the Francisella-like endosymbionts of Dermacentor ticks. J Med Entomol 41:277–286CrossRefPubMedGoogle Scholar
  83. Simser JA, Palmer AT, Fingerle V, Wilske B, Kurtti TJ, Munderloh UG (2002) Rickettsia monacensis sp. nov., a spotted fever group rickettsia, from ticks (Ixodes ricinus) collected in a European city park. Appl Environ Microbiol 68:4559–4566CrossRefPubMedGoogle Scholar
  84. Subramanian G, Sekeyova Z, Raoult D, Mediannikov O (2012) Multiple tick associated bacteria in Ixodes ricinus from Slovakia. Ticks Tick Borne Dis 3(5–6):406–410CrossRefPubMedGoogle Scholar
  85. Sun LV, Scoles GA, Fish D, O’Neill SL (2000) Francisella-like endosymbionts of ticks. J Invertebr Pathol 76:301–303CrossRefPubMedGoogle Scholar
  86. Taylor M, Mediannikov O, Raoult D, Greub G (2012) Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol Med Microbiol 64:21–31CrossRefPubMedGoogle Scholar
  87. Telford SR, Goethert HK (2004) Emerging tick-borne infections: rediscovered and better characterized, or truly ‘new’? Parasitology 129:s301–s327CrossRefPubMedGoogle Scholar
  88. Thao ML, Baumann P (2004) Evidence for multiple acquisition of Arsenophonus by whitefly Species (Sternorrhycha: Aleyrodidae). Curr Microbiol 48:140–144CrossRefPubMedGoogle Scholar
  89. Venzal JM, Estrada-Peña A, Castro O, de Souza CG, Félix ML, Nava S, Guglielmone AA (2008) Amblyomma triste Koch, 1844 (Acari: Ixodidae): hosts and seasonality of the vector of Rickettsia parkeri in Uruguay. Vet Parasitol 155:104–109Google Scholar
  90. Weller SJ, Baldridge GD, Munderloh UG, Noda H, Simser J, Kurtti TJ (1998) Phylogenetic placement of rickettsiae from the ticks Amblyomma americanum and Ixodes scapularis. J Clin Microbiol 36:1305–1317PubMedGoogle Scholar
  91. Williams-Newkirk AJ, Rowe LA, Mixson-Hayden TR, Dasch GA (2012) Presence, genetic variability, and potential significance of "Candidatus Midichloria mitochondrii" in the lone star tick Amblyomma americanum. Exp Appl Acarol 58:291–300CrossRefPubMedGoogle Scholar
  92. Yuasa Y, Yoshiie K, Takasaki T, Yoshida H, Oda H (1996) Retrospective survey of chronic Q fever in Japan by using PCR to detect Coxiella burnetii DNA in paraffin- embedded clinical samples. J Clin Microbiol 34:824–827PubMedGoogle Scholar
  93. Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016CrossRefPubMedGoogle Scholar
  94. Zhang GQ, Hotta A, Mizutani M, Ho T, Yamaguchi T, Fukushi H, Hirai K (1998) Direct identification of Coxiella burnetii plasmids in human sera by nested PCR. J Clin Microbiol 36:2210–2213PubMedGoogle Scholar
  95. Zhang X, Norris DE, Rasgon JL (2011) Distribution and molecular characterization of Wolbachia endosymbionts and filarial nematodes in Maryland populations of the lone star tick (Amblyomma americanum). FEMS Microbiol Ecol 77:50–56CrossRefPubMedGoogle Scholar
  96. Zhong J, Jasinskas A, Barbour AG (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS One 2:e405CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2013

Authors and Affiliations

  • Arunee Ahantarig
    • 1
    • 2
  • Wachareeporn Trinachartvanit
    • 1
  • Visut Baimai
    • 1
    • 2
  • Libor Grubhoffer
    • 3
  1. 1.Biodiversity Research Cluster, Department of Biology, Faculty of ScienceMahidol UniversityBangkokThailand
  2. 2.Center of Excellence for Vectors and Vector-Borne Diseases, Faculty of ScienceMahidol University at SalayaNakhon PathomThailand
  3. 3.Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic & Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic

Personalised recommendations