Characterization of the bacterial communities of life stages of free living lone star ticks (Amblyomma americanum)

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Williams Newkirk, Amanda Jo ^a,b,c   Rowe, Lori A ^d   Mixson Hayden, Tonya R ^d   Dasch, Gregory A ^c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

AMBLYOMMA AMERICANUM; ARTICLE; BACILLALES; BORRELIA; COXIELLA; DNA EXTRACTION; EHRLICHIA; ENTEROBACTERIACEAE; FEMALE; MALE; MICROBIAL COMMUNITY; MIDICHLORIA; MIXED INFECTION; NONHUMAN; NYMPH; PSEUDOMONAS; PYROSEQUENCING; RHIZOBIALES; RICKETTSIA; SYMBIONT; UNITED STATES; WOLBACHIA; ANIMAL; BACTERIA; CLASSIFICATION; DNA BARCODING; DNA SEQUENCE; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IXODIDAE; LIFE CYCLE STAGE; METAGENOMICS; MICROBIOLOGY; PARASITE VECTOR; PROCEDURES;

ANIMALS; ARTHROPOD VECTORS; BACTERIA; DNA BARCODING, TAXONOMIC; ECOSYSTEM; FEMALE; HUMANS; IXODIDAE; LIFE CYCLE STAGES; MALE; METAGENOMICS; NYMPH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84904602847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102130     Document Type: Article

References (73)

1. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129: S3-S14. doi:10.1017/S0031182004005967. (Pubitemid 40789958)
2. Merten HA, Durden LA (2000) A state-by-state survey of ticks recorded from humans in the United States. J Vector Ecol 25: 102-113.
3. Ginsberg HS, Ewing CP, O'Connell AF, Bosler EM, Daley JG, et al. (1991) Increased population densities of Amblyomma americanum (Acari: Ixodidae) on Long Island, New York. J Parasitol 77: 493-495. doi:10.2307/3283144.
4. Keirans JE, Lacombe EH (1998) First records of Amblyomma americanum, Ixodes (Ixodes) dentatus, and Ixodes (Ceratixodes) uriae (Acari: Ixodidae) from Maine. J Parasitol 84: 629-631. doi:10.2307/3284739. (Pubitemid 28280678)
5. Means RG, White DJ (1997) New distribution records of Amblyomma americanum (L.) (Acari: Ixodidae) in New York State. J Vector Ecol 22: 133-145. (Pubitemid 127525599)
6. Childs JE, Paddock CD (2003) The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol 48: 307-337. doi:10.1146/annurev.ento.48.091801.112728. (Pubitemid 37374923)
7. Buller RS, Arens M, Hmiel SP, Paddock CD, Sumner JW, et al. (1999) Ehrlichia ewingii, a newly recognized agent of human ehrlichiosis. N Engl J Med 341: 148-155. doi:10.1056/NEJM199907153410303. (Pubitemid 29325742)
8. 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: 291-300. doi:10.1007/s10493-012-9582-5.
9. Bazzocchi C, Mariconti M, Sassera D, Rinaldi L, Martin E, et al. (2013) Molecular and serological evidence for the circulation of the tick symbiont Midichloria (Rickettsiales: Midichloriaceae) in different mammalian species. Parasit Vectors 6: 1-7. doi:10.1186/1756-3305-6-350.
10. James AM, Liveris D, Wormser GP, Schwartz I, Montecalvo MA, et al. (2001) Borrelia lonestari infection after a bite by an Amblyomma americanum tick. J Infect Dis 183: 1810-1814. doi:10.1086/320721. (Pubitemid 32523246)
11. Kokernot RH, Calisher CH, Stannard LJ, Hayes J (1969) Arbovirus studies in the Ohio-Mississippi basin, 1964-1967 VII. Lone Star virus, a hitherto unknown agent isolated from the tick Amblyomma americanum (Linn.). Am J Trop Med Hyg 18: 789-795.
12. Savage HM, Godsey MS, Lambert A, Panella NA, Burkhalter KL, et al. (2013) First detection of Heartland virus (Bunyaviridae: Phlebovirus) from field collected arthropods. Am J Trop Med Hyg 89: 445-452. doi:10.4269/ajtmh.13-0209.
13. Gladney WJ, Drummond RO (1970) Mating behavior and reproduction of the lone star tick, Amblyomma americanum. Ann Entomol Soc Am 63: 1036-1039.
14. Mixson TR, Campbell SR, Gill JS, Ginsberg HS, Reichard MV, et al. (2006) Prevalence of Ehrlichia, Borrelia, and rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine states. J Med Entomol 43: 1261-1268. doi:10.1603/0022-2585(2006)43[1261:POEBAR]2.0.CO;2. (Pubitemid 44862962)
15. Corrigan J (2012) Investigation of spotted fever group Rickettsia in dogs and ticks in northern California. MS Thesis, Humboldt State University. Available: http://humboldt-dspace.calstate.edu/handle/2148/980?show=full. Accessed 2013 December 31.
16. Clay K, Klyachko O, Grindle N, Civitello D, Oleske D, et al. (2008) Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol Ecol 17: 4371-4381. doi:10.1111/j.1365-294X.2008.03914.x.
17. Heise SR, Elshahed MS, Little SE (2010) Bacterial diversity in Amblyomma americanum (Acari: Ixodidae) with a focus on members of the genus Rickettsia. J Med Entomol 47: 258-268. doi:10.1603/me09197.
18. Ponnusamy L, Gonzalez A, Treuren WV, Weiss S, Parobek CM, et al. (2014) Diversity of Rickettsiales in the microbiome of the lone star tick, Amblyomma americanum. Appl Environ Microbiol 80: 354-359. doi:10.1128/AEM.02987-13.
19. Yuan D (2010) A metagenomic study of the tick midgut. MS Thesis, The University of Texas. Available: http://digitalcommons.library.tmc.edu/utgsbs- dissertations/85. Accessed 2013 July 17.
20. Jasinskas A, Zhong J, Barbour AG (2007) Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl Environ Microbiol 73: 334-336. doi:10.1128/aem.02009-06. (Pubitemid 46079968)
21. Zhong JM, Jasinskas A, Barbour AG (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS One 2: e405. doi:10.1371/journal.pone.0000405.
22. Menchaca AC, Visi DK, Strey OF, Teel PD, Kalinowski K, et al. (2013) Preliminary assessment of microbiome changes following blood-feeding and survivorship in the Amblyomma americanum nymph-to-adult transition using semiconductor sequencing. PLoS ONE 8: e67129. doi:10.1371/journal.pone.0067129.
23. Moreno CX, Moy F, Daniels TJ, Godfrey HP, Cabello FC (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.
24. Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, et al. (2013) The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J 7: 221-223. doi:10.1038/ismej.2012.71.
25. Lalzar I, Harrus S, Mumcuoglu KY, Gottlieb Y (2012) Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl Environ Microbiol 78: 4110-4116. doi:10.1128/AEM.00323-12.
26. Halos L, Bord S, Cotté V, Gasqui P, Abrial D, et al. (2010) Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol 76: 4413-4420. doi:10.1128/AEM.00610-10.
27. Lo N, Beninati T, Sassera D, Bouman EAP, Santagati S, et al. (2006) Widespread distribution and high prevalence of an alpha-proteobacterial symbiont in the tick Ixodes ricinus. Environ Microbiol 8: 1280-1287. doi:10.1111/j.1462-2920.2006.01024.x. (Pubitemid 43901758)
28. Bermúdez SE, Eremeeva ME, Karpathy SE, Samudio F, Zambrano ML, et al. (2009) Detection and identification of rickettsial agents in ticks from domestic mammals in eastern Panama. J Med Entomol 46: 856-861. doi:10.1603/033.046.0417.
29. Hartmann C, Lennartz K, Ibrahim H, Coz A, Kasper Y, et al. (8/20102) Application Note: Stable 16-year Storage of DNA Purified with the QIAamp DNA Blood Mini Kit. Available: http://www.qiagen.com/knowledge-and-support/resource- center/resource-download.aspx?id=705c6944-4633-4101-8500-a6642d253a0e&lang= en. Accessed 2014 April 6.
30. Jumpstart Consortium Human Microbiome Project Data Generation Working Group (2010) 16S 454 Sequencing Protocol HMP Consortium (version 4.2.2). Available: http://www.hmpdacc.org/doc/16S-Sequencing-SOP-4.2.2.pdf. Accessed 2014 April 6.
31. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541. doi:10.1128/AEM.01541-09.
32. Schloss PD (2013) Schloss SOP. Mothur Wiki. Available: http://www.mothur.org/wiki/Schloss-SOP. Accessed 2013 September 30.
33. Schloss PD (2009) A high-throughput DNA sequence aligner for microbial ecology studies. PLoS ONE 4: e8230. doi:10.1371/journal.pone.0008230.
34. Zhou J, Wu L, Deng Y, Zhi X, Jiang Y-H, et al. (2011) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5: 1303-1313. doi:10.1038/ismej.2011.11.
35. Esty WW (1986) The efficiency of Good's nonparametric coverage estimator. Ann Stat 14: 1257-1260. doi:10.1214/aos/1176350066.
36. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43: 1-11. doi:10.1111/j.1574-6941.2003.tb01040.x. (Pubitemid 36173508)
37. Pinto AJ, Raskin L (2012) PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS ONE 7: e43093. doi:10.1371/journal.pone.0043093.
38. R Core Team (2013) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: http://www.R-project.org.
39. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Société Vaudoise Sci Nat 44: 223-270.
40. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27: 326-349. doi:10.2307/1942268.
41. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2013) vegan: Community Ecology Package. Available: http://cran.r-project.org/web/ packages/vegan/index.html.
42. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
43. Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69: 57-68. doi:10.2307/ 20038103.
44. Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69: 89-107. doi:10.2307/20038106.
45. Kindt R, Coe R (2005) Chapter 10: analysis of ecological distance by ordination. Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. Nairobi, Kenya: World Agroforestry Centre. 153-196.
46. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352. doi:10.1371/journal.pcbi.1000352.
47. Pawitan Y, Michiels S, Koscielny S, Gusnanto A, Ploner A (2005) False discovery rate, sensitivity and sample size for microarray studies. Bioinformatics 21: 3017-3024. doi:10.1093/bioinformatics/bti448. (Pubitemid 40916427)
48. Bartlett MS (1937) Properties of sufficiency and statistical tests. Proc R Soc Lond Ser A 160: 268-282.
49. Veech JA (2013) A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr 22: 252-260. doi:10.1111/j.1466-8238.2012. 00789.x.
50. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46. doi:10.1111/j.1442-9993.2001.01070.pp.x.
51. Hong S, Bunge J, Leslin C, Jeon S, Epstein SS (2009) Polymerase chain reaction primers miss half of rRNA microbial diversity. ISME J 3: 1365-1373. doi:10.1038/ismej.2009.89.
52. Berry D, Mahfoudh KB, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 77: 7846-7849. doi:10.1128/AEM.05220-11.
53. Acinas SG, Sarma-Rupavtarm R, Klepac-Ceraj V, Polz MF (2005) PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl Environ Microbiol 71: 8966-8969. doi:10.1128/AEM.71.12.8966-8969.2005. (Pubitemid 41804041)
54. Clay K, Fuqua C (2010) The tick microbiome: diversity, distribution and influence of the internal microbial community for a blood-feeding disease vector. Critical Needs and Gaps in Understanding Prevention, Amelioration, and Resolution of Lyme and Other Tick-Borne Diseases: The Short-Term and Long-Term Outcomes. Washington, D. C.: Institute of Medicine Committee on Lyme Disease and Other Tick-Borne Diseases: The State of the Science. Available: iom.edu/∼/media/Files/Activity%20Files/Disease/TickBorne/ 08-The-Tick-Microbiome.pdf.
55. Kauserud H, Kumar S, Brysting AK, Nordén J, Carlsen T (2012) High consistency between replicate 454 pyrosequencing analyses of ectomycorrhizal plant root samples. Mycorrhiza 22: 309-315. doi:10.1007/s00572-011-0403-1.
56. Pilloni G, Granitsiotis MS, Engel M, Lueders T (2012) Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to T-RFLP fingerprinting of aquifer microbes. PLoS ONE 7: e40467. doi:10.1371/journal.pone.0040467.
57. Moncayo AC, Cohen SB, Fritzen CM, Huang E, Yabsley MJ, et al. (2010) Absence of Rickettsia rickettsii and occurrence of other spotted fever group rickettsiae in ticks from Tennessee. Am J Trop Med Hyg 83: 653-657. doi:10.4269/ajtmh.2010.09-0197.
58. Fritzen CM, Huang J, Westby K, Freye JD, Dunlap B, et al. (2011) Infection prevalences of common tick-borne pathogens in adult lone star ticks (Amblyomma americanum) and American dog ticks (Dermacentor variabilis) in Kentucky. Am J Trop Med Hyg 85: 718-723. doi:10.4269/ajtmh.2011.10-0583.
59. Klyachko O, Stein BD, 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: 6584-6594. doi:10.1128/AEM.00537-07. (Pubitemid 47623718)
60. Jiang J, Yarina T, Miller MK, Stromdahl EY, Richards AL (2010) Molecular detection of Rickettsia amblyommii in Amblyomma americanum parasitizing humans. Vector-Borne Zoonotic Dis 10: 329-340. doi:10.1089/vbz.2009.0061.
61. Zhang X, Ren X, Norris DE, Rasgon JL (2012) Distribution and infection frequency of "Candidatus Rickettsia amblyommii" in Maryland populations of the lone star tick (Amblyomma americanum) and culture in an Anopheles gambiae mosquito cell line. Ticks Tick-Borne Dis 3: 38-42. doi:10.1016/j.ttbdis.2011.09.010.
62. Dasch G, Kelly D, Richards A, Sanchez J, Rives C (1993) Western blotting analysis of sera from military personnel exhibiting serological reactivity to spotted fever group rickettsiae. Am J Trop Med Hyg 49: 220.
63. Apperson CS, Engber B, Nicholson WL, Mead DG, Engel J, et al. (2008) Tickborne diseases in North Carolina: is "Rickettsia amblyommii" a possible cause of rickettsiosis reported as Rocky Mountain spotted fever? Vector-Borne Zoonotic Dis 8: 597-606. doi:10.1089/vbz.2007.0271.
64. Billeter SA, Blanton HL, Little SE, Levy MG, Breitschwerdt EB (2007) Detection of "Rickettsia amblyommii" in association with a tick bite rash. Vector-Borne Zoonotic Dis 7: 607-610. doi:10.1089/vbz.2007.0121.
65. Stromdahl EY, Vince MA, Billingsley PM, Dobbs NA, Williamson PC (2008) Rickettsia amblyommii infecting Amblyomma americanum larvae. Vector-Borne Zoonotic Dis 8: 15-24. doi:10.1089/vbz.2007.0138. (Pubitemid 351271596)
66. Smith MP, Ponnusamy L, Jiang J, Ayyash LA, Richards AL, et al. (2010) Bacterial pathogens in ixodid ticks from a Piedmont county in North Carolina: prevalence of rickettsial organisms. Vector-Borne Zoonotic Dis 10: 939-952. doi:10.1089/vbz.2009.0178.
67. Zanetti AS, Pornwiroon W, Kearney MT, Macaluso KR (2008) Characterization of rickettsial infection in Amblyomma americanum (Acari: Ixodidae) by quantitative real-time polymerase chain reaction. J Med Entomol 45: 267-275. doi:10.1603/0022-2585(2008)45[267:CORIIA]2.0.CO;2.
68. Kagemann J, Clay K (2013) Effects of infection by Arsenophonus and Rickettsia bacteria on the locomotive ability of the ticks Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis. J Med Entomol 50: 155-162. doi:10.1603/ME12086.
69. 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: 50-56. doi:10.1111/j.1574-6941.2011.01089.x.
70. Baldo L, Prendini L, Corthals A, Werren JH (2007) Wolbachia are present in southern African scorpions and cluster with supergroup F. Curr Microbiol 55: 367-373. doi:10.1007/s00284-007-9009-4. (Pubitemid 47536827)
71. Covacin C, Barker SC (2007) Supergroup F Wolbachia bacteria parasitise lice (Insecta: Phthiraptera). Parasitol Res 100: 479-485. doi:10.1007/s00436- 006-0309-6. (Pubitemid 46011258)
72. Casiraghi M, Favia G, Cancrini G, Bartoloni A, Bandi C (2001) Molecular identification of Wolbachia from the filarial nematode Mansonella ozzardi. Parasitol Res 87: 417-420. doi:10.1007/s004360000368. (Pubitemid 32391446)
73. Lefoulon E, Gavotte L, Junker K, Barbuto M, Uni S, et al. (2012) A new type F Wolbachia from Splendidofilariinae (Onchocercidae) supports the recent emergence of this supergroup. Int J Parasitol 42: 1025-1036. doi:10.1016/j.ijpara.2012.09.004.