Bacterial diversity in amblyomma americanum (Acari: Ixodidae) with a focus on members of the genus rickettsia

Journal of Medical Entomology

Volumn 47, Issue 2, 2010, Pages 258-268

  Heise, Stephanie R ^a   Elshahed, M S ^a   Little, S E ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

16S gene; Amblyomma americanum; Bacterial diversity; Rickettsia

Indexed keywords

BACTERIAL RNA; RNA 16S;

ANIMAL; ARTICLE; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; RICKETTSIA; TICK;

ANIMALS; IXODIDAE; PHYLOGENY; RICKETTSIA; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

ACARI; AMBLYOMMA AMERICANUM; ANIMALIA; BACTERIA (MICROORGANISMS); BREVIBACTERIUM; COXIELLA; IXODIDA; IXODIDAE; OTUS; RICKETTSIA; RICKETTSIA AMBLYOMMII; RICKETTSIA MASSILIAE; RICKETTSIA SP.; RICKETTSIALES;

EID: 77949279987     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME09197     Document Type: Article

References (76)

1. Altschul, S., T. Madden, A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. Lipman. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389-3402.
2. Anderson, B. E., J. E. Dawson, D. C. Jones, and K. H. Wilson. 1991. Ehrlichia chaffeensis, a new species associated with human ehrlichiosis. J. Clin. Microb. 29: 2838-2842.
3. Anderson, B. E., C. E. Greene, D. C. Jones, and J. E. Dawson. 1992a. NOTES: Ehrlichia ewingii sp. nov., the etiologic agent of canine granulocytic ehrlichiosis. Int. J. Syst. Bacteriol. 42: 299-302.
4. Anderson, B. E., J. W. Sumner, J. E. Dawson, T. Tzianabos, C. R. Greene, J. G. Olson, D. B. Fishbein, M. Olsen-Rasmussen, B. P. Holloway, and E. H. George. 1992b. Detection of the etiologic agent of human ehrlichiosis by polymerase chain reaction. J. Clin. Microb. 30: 775-780.
5. Apperson, C. S., B. Engber, W. L. Nicholson, D. G. Mead, J. Engel, M. J. Yabsley, K. Dail, J. Johnson, and D. W. Watson. 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: 1-9.
6. Azad, A. F., and C. B. Beard. 1998. Rickettsial pathogens and their arthropod vectors. Emerg. Infect. Dis. 4: 179-186.
7. Bacon, R. M., M. A. Pilgard, B.J.B. Johnson, J. Piesman, B. J. Biggerstaff, and M. Quintana. 2005. Rapid detection methods and prevalence estimation for Borrelia lonestari glpQ in Amblyomma americanum (Acari: Ixodidae) pools of unequal size. Vector Borne Zoonotic Dis. 5: 146-156.
8. Barbour, A. G., G. O. Maupin, G. J. Teltow, C. J. Carter, and J. Piesman. 1996. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like Illness. J. Infect. Dis. 173: 403-409.
9. Benson, M. J., J. D. Gawronski, D. E. Eveleigh, and D. R. Benson. 2004. Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellßeet, Cape Cod, Massachusetts. Appl. Environ. Microbiol. 70: 616-620.
10. Billeter, S.A.B., L. Hunter, S. E. Little, M. G. Levy, E. B. Breitschwerdt. 2007. Detection of "Rickettsia amblyommii" in association with a tick bite rash. Vector Borne Zoonotic Dis. 7: 607-610.
11. Blanc, G., H. Ogata, C. Robert, S. P. Audic, J.-M. Claverie, and D. Raoult. 2007. Lateral gene transfer between obligate intracellular bacteria: evidence from the Rickettsia massiliae genome. Genome Res. 17: 1657-1664.
12. Blanton, L., B. Keith, and W. Brzezinski. 2008. Southern tick-associated rash illness: erythema migrans is not always Lyme disease. South. Med. J. 101: 759-760.
13. Buller, R. S., M. Arens, S. P. Hmiel, and C. D. Paddock. 1999. Ehrlichia ewingii, a newly recognized agent of human ehrlichiosis. N. Engl. J. Med. 341: 148-155.
14. Burgdorfer, W. 1969. Ecology of tick vectors of American spotted fever. Bull. W.H.O. 40: 375-381.
15. [CDC] Centers for Disease Control. 1997. Case definitions for infectious conditions under public health surveillance., pp. RR-10. MMWR.
16. Childs, J. E., and C. D. Paddock. 2003. The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu. Rev. Entomol. 48: 307-337.
17. Clay, K., N. Klyachko, D. Grindle, D. Oleske, D. Civitello, and C. Fuqua. 2008. Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol. Ecol. 17: 4371-4381.
18. Crossman, L., V. Gould, J. M. Dow, G. Vernikos, A. Okazaki, M. Sebaihia, D. Saunders, C. Arrowsmith, T. Carver, N. Peters, E. Adlem, A. Kerhornou, A. Lord, L. Murphy, K. Seeger, R. Squares, S. Rutter, M. Quail, M.-A. Rajandream, D. Harris, C. Churcher, S. Bentley, J. Parkhill, N. Thomson, and M. Avison. 2008. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol. 9: R74.
19. Dawson, J. E., K. L. Biggie, C. K. Warner, K. Cookson, S. Jenkens, J. F. Levine, and J. G. Olson. 1996. Polymerase chain reaction evidence of Ehrlichia chaffeensis, an etiologic agent of human ehrlichiosis, in dogs from southeast Virginia. Am. J. Vet. Res. 57: 1175-1179.
20. Demma, L. J., M. Traeger, D. Blau, R. Gordon, B. Johnson, J. Dickson, R. Ethelbah, S. Piontkowski, C. Levy, W. L. Nicholson, C. Duncan, K. Heath, J. Cheek, D. L. Swerdlow, and J. H. McQuiston. 2006. Serologic evidence for exposure to Rickettsia rickettsii in eastern Arizona and recent emergence of Rocky Mountain Spotted Fever in this region. Vector Borne Zoonotic Dis. 6: 423-429.
21. DeSantis, T. Z., P. Hugenholtz, N. Larsen, M. Rojas, E. L. Brodie, K. Keller, T. Huber, D. Dalevi, P. Hu, and G. L. Andersen. 2006a. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072.
22. DeSantis, T. Z., Jr., P. Hugenholtz, K. Keller, E. L. Brodie, N. Larsen, Y. M. Piceno, R. Phan, and G. L. Andersen. 2006b. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucl. Acids Res. 34: W394-399.
23. de Silva, A. M., and E. Fikrig. 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 53: 397-404.
24. Dojka, M. A., P. Hugenholtz, S. K. Haack, and N. R. Pace. 1998. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64: 3869-3877.
25. Elshahed, M.S.S., S. John, F. Z. Najar, S. M. Kenton, B. A. Roe, T. A. Dewers, J. Spear, and L. R. Krumholz. 2003. Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring. Appl. Environ. Microbiol. 69: 5609-5621.
26. Eremeeva, M. E., E. A. Bosserman, L. J. Demma, M. L. Zambrano, D. M. Blau, and G. A. Dasch. 2006. Isolation and identification of Rickettsia massiliae from Rhipicephalus sanguineus ticks collected in Arizona. Appl. Environ. Microbiol. 72: 5569-5577.
27. Ewing, S. A., W. R. Roberson, R. G. Buckner, and C. S. Hayat. 1971. A new strain of Ehrlichia canis. J. Am. Vet. Med. Assoc. 159: 1771-1774.
28. Felz, M. W., L. A. Durden, and J. H. Oliver, Jr. 1996. Ticks parasitizing humans in Georgia and South Carolina. J. Parasitol. 82: 505-508.
29. Fernandez-Soto, P., R. Perez-Sanchez, V. Diaz Martin, A. Encinas-Grandes, and R. Alamo Sanz. 2006. Rickettsia massiliae in ticks removed from humans in Castilla y Leó n, Spain. Eur. J. Clin. Micribiol. Infect. Dis. 25: 811- 813. (Pubitemid 44786659)
30. Fournier, P.-E., N. Takada, H. Fujita, and D. Raoult. 2006. Rickettsia tamurae sp. nov., isolated from Amblyomma testudinarium ticks. Int. J. Syst. Evol. Microbiol. 56: 1673- 1675.
31. Fujita, H., P.-E. Fournier, N. Takada, T. Saito, and D. Raoult. 2006. Rickettsia asiatica sp. nov., isolated in Japan. Int. J. Syst. Evol. Microbiol. 56: 2365-2368.
32. Ginsberg, H. S., M. Butler, and E. Zhioua. 2002. Effect of deer exclusion by fencing on abundance of Amblyomma americanum (Acari: Ixodidae) on Fire Island, New York, USA. J. Vector Ecol. 27: 215-221.
33. Goddard, J., and B. R. Norment. 1986. Spotted fever group Rickettsiae in the lone star tick, Amblyomma americanum (Acari: Ixodidae). J. Med. Entomol. 23: 465-472.
34. Good, I. J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237-264.
35. Guedes, E., R. C. Leite, M.C.A. Prata, R. C. Pacheco, D. H. Walker, and M. B. Labruna. 2005. Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais. Mem. Inst. Oswaldo Cruz. 100: 841-845.
36. James, A. M., D. Liveris, G. P. Wormser, I. Schwartz, M. A. Montecalvo, and B.J.B. Johnson. 2001. Borrelia lonestari infection after a bite by an Amblyomma americanum tick. J. Infect. Dis. 183: 1810-1814.
37. Jasinskas, A., J. Zhong, and A. G. Barbour. 2007. Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl. Environ. Microbiol. 73: 334- 336.
38. Keirans, J. E., and E. H. Lacombe. 1998. First records of Amblyomma americanum, Ixodes (Ixodes) dentatus, and Ixodes (Ceratixodes) uriae (Acari: Ixodidae) from Maine. J. Parasitol. 84: 629-631.
39. Kirkland, K. B., T. B. Klimko, R. A. Meriwether, M. Schriefer, M. Levin, J. Levine, W.R.M. Kenzie, and D. T. Dennis. 1997. Erythema migrans-like rash illness at a camp in North Carolina: a new tick-borne disease? Arch. Intern. Med. 157: 2635-2641.
40. Klyachko, O., B. D. Stein, N. Grindle, K. Clay, and C. Fuqua. 2007. Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl. Environ. Microbiol. 73: 6584-6594.
41. Lockhart, J. M., W. R. Davidson, D. E. Stallknecht, J. E. Dawson, and S. E. Little. 1997. Natural history of Ehrlichia chaffeensis (Rickettsiales: Ehrlichieae) in the Piedmont physiographic province of Georgia. J. Parasitol. 83: 887-894.
42. Looney, W. J., M. Narita, and K. Mühlemann. 2009. Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect. Dis. 9: 312-323.
43. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucl. Acids Res. 32: 1363-1371.
44. Macaluso, K. R., D. E. Sonenshine, S. M. Cearul, and A. F. Azad. 2001. Infection and transovarial transmission of Rickettsiae in Dermacentor variabilis ticks acquired by artificial feeding. Vector Borne Zoonotic Dis. 1: 45-53.
45. Magurran, A. E. 2004. Measuring biological diversity. Blackwell Ltd., Oxford, United Kingdom.
46. Manangan, J. S., S. H. Schweitzer, N. Nibbelink, M. J. Yabsley, S.E.J. Gibbs, and M. C. Wimberly. 2007. Habitat factors inßuencing distributions of Anaplasma phagocytophilum and Ehrlichia chaffeensis in the Mississippi Alluvial Valley. Vector Borne Zoonotic Dis. 7: 563-574.
47. Martin, A. P. 2002. Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl. Environ. Microbiol. 68: 3673-3682.
48. Masters, E. J., C. N. Grigery, and R. W. Masters. 2008. STARI, or masters disease: lone star tick-vectored Lymelike illness. Infect. Dis. Clin. North Am. 22: 361-376.
49. McDade, J. E., and V. F. Newhouse. 1986. Natural History of Rickettsia rickettsii. Annu. Rev. Microbiol. 40: 287-309.
50. McQuiston, J. H., C. L. McCall, and W. L. Nicholson. 2003. Ehrlichiosis and related infections. J. Am. Vet. Med. Assoc. 223: 1750-1756.
51. Mediannikov, O., K. Matsumoto, I. Samoylenko, M. Drancourt, V. Roux, E. Rydkina, B. Davoust, I. Tarasevich, P. Brouqui, and P.-E. Fournier. 2008. Rickettsia raoultii sp. nov., a spotted fever group rickettsia associated with Dermacentor ticks in Europe and Russia. Int. J. Syst. Evol. Microbiol. 58: 1635-1639.
52. Miura, K., and Y. Rikihisa. 2007. Virulence potential of Ehrlichia chaffeensis strains of distinct genome sequences. Infect. Immunol. 75: 3604-3613.
53. Mixson, T. R., S. R. Campell, J. S. Gill, H. S. Ginsberg, M. V. Reichard, T. L. Schulze, and G. A. Dasch. 2006. Prevalence of Ehrlichia, Borrelia, and Rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine States. J. Med. Entomol. 43: 1261-1268.
54. Moreno, C. X., F. Moy, T. J. Daniels, H. P. Godfrey, and F. C. Cabello. 2006. Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess Counties, New York. Environ. Microbiol. 8: 761-772.
55. Nicholson, W. L., E. Masters, and G. P. Wormser. 2009. Preliminary serologic investigation of ÔRickettsia amblyommii Õ in the etiology of southern tick-associated rash illness (STARI). Clin. Microbiol. Infect. 15: 235-236.
56. Ogawa, M., K. Matsumoto, P. Philippe, D. B. Raoult, and P. Brouqui. 2006. Expression of rOmpA and rOmpB protein in Rickettsia massiliae during the Rhipicephalus turanicus life cycle. Ann. N. Y. Acad. Sci. 1078: 352-356.
57. Olano, J. P., E. J. Masters, W. Hogrefe, and D. H. Walker. 2003. Human monocytotropic ehrlichiosis, Missouri. Emerg. Infect. Dis. 9: 1579-1586.
58. Paddock, C. D., and M. J. Yabsley. 2007. Ecological havoc, the rise of white-tailed deer, and the emergence of Amblyomma americanum-associated zoonoses in the United States. Curr. Top. Microbiol. Immunol. 315: 289-324.
59. Parola, P., M. B. Labruna, and D. Raoult. 2009. Tick-borne Rickettsioses in America: unanswered questions and emerging diseases. Curr. Infect. Dis. Rep. 11: 40-50.
60. Pascual, C., and M. D. Collins. 1999. Brevibacterium avium sp. nov., isolated from poultry. Int. J. Syst. Bacteriol. 49: 1527-1530.
61. Philipp, M. T., E. Masters, G. P. Wormser, W. Hogrefe, and D. Martin. 2006. Serologic evaluation of patients from Missouri with erythema migrans-like skin lesions with the C6 Lyme test. Clin. Vaccine Immunol. 13: 1170-1171.
62. Reeves, W. K., A. D. Loftis, W. L. Nicholson, and A. G. Czarkowski. 2008. The first report of human illness associated with the Panola Mountain Ehrlichia species: a case report. J. Med. Case Reports. 2: 139.
63. Regnery, R. L., C. L. Spruill, and B. D. Plikaytis. 1991. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J. Bacteriol. 173: 1576-1589.
64. Schloss, P. D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71: 1501-1506.
65. Schloss, P. D., and J. Handelsman. 2006. Toward a census of bacteria in soil. PLoS Comput. Biol. 2: 786-793.
66. Stothard, D. 1995. The evolutionary history of the genus Rickettsia as inferred from 16S and 23S ribosomal RNA genes and the 17 kilodalton cell surface antigen gene, pp. 214. Department of Molecular Genetics, The Ohio State University, Columbus, OH.
67. Strohmdahl, E. Y., P. C. Williamson, M. A. Vince, N. A. Dobbs, and P. M. Billingsley. 2008. Rickettsia amblyommii infecting Amblyomma americanum larvae. Vector Borne Zoonotic Dis. 8: 15-24.
68. Thompson, J., T. Gibson, F. Plewniak, F. Jeanmougin, and D. Higgins. 1997. The CLUSTAL X windows interface: ßexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25: 4876-4882.
69. Toleman, M. A., P. M. Bennett, D.M.C. Bennett, R. N. Jones, and T. R. Walsh. 2007. Global emergence of trimethoprim/ sulfamethoxazole resistance in Stenotrophomonas maltophilia mediated by acquisition of sul genes. Emerg. Infect. Dis. 13: 559-565.
70. Varela, A. S., V. A. Moore, and S. E. Little. 2004. Disease agents in Amblyomma americanum from northeastern Georgia. J. Med. Entomol. 41: 753-759.
71. Wimberly, M., A. Baer, and M. Yabsley. 2008. Enhanced spatial models for predicting the geographic distributions of tick-borne pathogens. Int. J. Health Geogr. 7: 15.
72. Wormser, G. P., E. Masters, D. Liveris, J. Nowakowski, D. Nadelman, D. Holmgren, S. Bittker, D. Cooper, G. Mang, and I. Schwartz. 2005a. Microbiologic evaluation of patients from Missouri with erythema migrans. CID. 40: 423-428.
73. Wormser, G. P., E. Masters, J. Nowakowski, D. McKenna, D. Holmgren, K. Ma, L. Ihde, L. F. Cavaliere, and R. B. Nadelman. 2005b. Prospective clinical evaluation of patients from Missouri and New York with erythema migrans-like skin lesions. CID. 41: 958-965.
74. Yabsley,M.J., A. D. Loftis, and S. E. Little. 2008. Natural and experimental infection of white-tailed deer (Odocoileus virginianus) from the United States with an Ehrlichia sp. closely related to Ehrlichia rumunantium. J. Wildl. Dis. 44: 381-387.
75. Zanetti, A. S., W. Pornwiroon, M. T. Kearney, and K. R. Macaluso. 2008. Characterization of rickettsial infection in Amblyomma americanum (Acari: Ixodidae) by quantitative real-time polymerase chain reaction. J. Med. Entomol. 45: 267-275.
76. Zhong, J., A. Jasinskas, and A. G. Barbour. 2007. Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS ONE. 2: e405.