Variation in the microbiota of Ixodes ticks with regard to geography, species, and sex

Applied and Environmental Microbiology

Volumn 81, Issue 18, 2015, Pages 6200-6209

  van Treuren, Will ^a   Ponnusamy, Loganathan ^b   Brinkerhoff, R Jory ^c,d   Gonzalez, Antonio ^e   Parobek, Christian M ^f   Juliano, Jonathan J ^f   Andreadis, Theodore G ^g   Falco, Richard C ^h   Ziegler, Lorenza Beati ⁱ   Hathaway, Nicholas ^j   Keeler, Corinna ^k   Emch, Michael ^k   Bailey, Jeffrey A ^j   Roe, R Michael ^b   Apperson, Charles S ^b,e   Knight, Rob ^e,j   Meshnick, Steven R ^a,l  

^a STANFORD UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF RICHMOND   (United States)

^d UNIVERSITY OF KWAZULU NATAL   (South Africa)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g The Connecticut Agricultural Experiment Station ^*  (United States)

^h NEW YORK STATE DEPARTMENT OF HEALTH   (United States)

ⁱ GEORGIA SOUTHERN UNIVERSITY   (United States)

^j UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^k University of North Carolina at Chapel Hill   (United States)

^l IL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGY; MICROBIOLOGY;

454-PYROSEQUENCING; ENTEROBACTERIACEAE; GEOGRAPHIC DIVERSITY; IXODES SCAPULARIS; PRINCIPAL VECTORS; SOUTH CAROLINA; SUBSTANTIAL VARIATIONS; UPPER MIDWESTS;

LOCATION;

BACTERIUM; GEOGRAPHICAL DISTRIBUTION; LYME DISEASE; MICROBIOLOGY; PATHOGEN; SPECIES DIVERSITY; TICK;

ATLANTIC COAST [NORTH AMERICA]; ATLANTIC COAST [UNITED STATES]; CONNECTICUT; MIDWEST; NEW YORK [UNITED STATES]; NORTH CAROLINA; SOUTH CAROLINA; UNITED STATES; VIRGINIA;

BORRELIA; ENTEROBACTERIACEAE; IXODES; IXODES AFFINIS; IXODES SCAPULARIS; IXODIDA; RICKETTSIA;

BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

ANIMAL; BACTERIUM; BIOTA; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; GEOGRAPHY; IXODES; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; SEX DIFFERENCE; UNITED STATES;

ANIMALS; BACTERIA; BIOTA; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; GEOGRAPHY; IXODES; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEX FACTORS; UNITED STATES;

EID: 84945271904     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01562-15     Document Type: Article

References (46)

1. Hinckley AF, Connally NP, Meek JI, Johnson BJ, Kemperman MM, Feldman KA, White JL, Mead PS. 2014. Lyme disease testing by large commercial laboratories in the United States. Clin Infect Dis 59:676-681. http://dx.doi.org/10.1093/cid/ciu397.
2. Layfield D, Guilfoile P. 2002. The prevalence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) and the agent of human granulocytic ehrlichiosis (Rickettsiaceae: Ehrlichieae) in Ixodes scapularis (Acari: Ixodidae) collected during 1998 and 1999 from Minnesota. J Med Entomol 39:218-220. http://dx.doi.org/10.1603/0022-2585-39.1.218.
3. Prusinski M, Kokas J, Hukey K, Kogut S, Lee J, Backenson P. 2014. Prevalence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae), Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae), and Babesia microti (Piroplasmida: Babesiidae) in Ixodes scapularis (Acari: Ixodidae) collected from recreational lands in the Hudson Valley Region, New York State. J Med Entomol 51:226-236. http://dx.doi.org/10.1603/ME13101.
4. 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. http://dx.doi.org/10.1111/j.1462-2920.2005.00955.x.
5. Adelson ME, Rao RV, Tilton RC, Cabets K, Eskow E, Fein L, Occi JL, Mordechai E. 2004. Prevalence of Borrelia burgdorferi, Bartonella spp., Babesia microti, and Anaplasma phagocytophila in Ixodes scapularis ticks collected in northern New Jersey. J Clin Microbiol 42:2799-2801. http: //dx.doi.org/10.1128/JCM.42.6.2799-2801.2004.
6. Eisen L, Eisen RJ, Mun J, Salkeld DJ, Lane RS. 2009. Transmission cycles of Borrelia burgdorferi and B. bissettii in relation to habitat type in northwestern California. J Vector Ecol 34:81-91. http://dx.doi.org/10.1111/j.1948-7134.2009.00010.x.
7. CDC. 2010. Lyme disease incidence rates by states, 2005-2009. CDC, Atlanta, GA.
8. Maggi RG, Reichelt S, Toliver M, Engber B. 2010. Borrelia species in Ixodes affinis and Ixodes scapularis ticks collected from the coastal plain of North Carolina. Ticks Tick-Borne Dis 1:168-171. http://dx.doi.org/10.1016/j.ttbdis.2010.08.003.
9. Clark KL, Oliver JH, Jr, James AM, Durden LA, Banks CW. 2002. Prevalence of Borrelia burgdorferi sensu lato infection among rodents and host-seeking ticks in South Carolina. J Med Entomol 39:198-206. http: //dx.doi.org/10.1603/0022-2585-39.1.198.
10. Harrison BA, Rayburn WH, Jr, Toliver M, Powell EE, Engber BR, Durden LA, Robbins RG, Prendergast BF, Whitt PB. 2010. Recent discovery of widespread Ixodes affinis (Acari: Ixodidae) distribution in North Carolina with implications for Lyme disease studies. J Vector Ecol 35:174-179. http://dx.doi.org/10.1111/j.1948-7134.2010.00074.x.
11. 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 17:4371-4381. http://dx.doi.org/10.1111/j.1365-294X 2008.03914.x.
12. Carpi G, Cagnacci F, Wittekindt NE, Zhao F, Qi J, Tomsho LP, Drautz DI, Rizzoli A, Schuster SC. 2011. Metagenomic profile of the bacterial communities associated with Ixodes ricinus ticks. PLoS One 6:e25604. http://dx.doi.org/10.1371/journal.pone.0025604.
13. Van Overbeek L, Gassner F, van der Plas CL, Kastelein P, Nunes-da Rocha U, Takken W. 2008. Diversity of Ixodes ricinus tick-associated bacterial communities from different forests. FEMS Microbiol Ecol 66: 72-84. http://dx.doi.org/10.1111/j.1574-6941.2008.00468.x.
14. Clay K, Fuqua C. 2010. The tick microbiome: diversity, distribution and influence of the internal microbial community for a blood-feeding disease vector. In Critical needs and gaps in understanding prevention, amelioration, and resolution of Lyme and other tick-borne diseases: the short-term and long-term outcomes. Workshop report. National Academies Press, Washington, DC.
15. Nakao R, Abe T, Nijhof AM, Yamamoto S, Jongejan F, Ikemura T, Sugimoto C. 2013. A novel approach, based on BLSOMs (batch learning self-organizing maps), to the microbiome analysis of ticks. ISME J 7:1003-1015. http://dx.doi.org/10.1038/ismej.2012.171.
16. Budachetri K, Browning RE, Adamson SW, Dowd SE, Chao C-C, Ching W-M, Karim S. 2014. An insight into the microbiome of the Amblyomma maculatum (Acari: Ixodidae). J Med Entomol 51:119-129. http://dx.doi.org/10.1603/ME12223.
17. Ponnusamy L, Gonzalez A, Van Treuren W, Weiss S, Parobek CM, Juliano JJ, Knight R, Roe RM, Apperson CS, Meshnick SR. 2014. Diversity of Rickettsiales in the microbiome of the lone star tick, Amblyomma americanum. Appl Environ Microbiol 80:354-359. http://dx.doi.org/10.1128/AEM. 02987-13.
18. Martin PA, Schmidtmann ET. 1998. Isolation of aerobic microbes from Ixodes scapularis (Acari: Ixodidae), the vector of Lyme disease in the eastern United States. J Econ Entomol 91:864-868. http://dx.doi.org/10.1093/jee/91.4.864.
19. Narasimhan S, Rajeevan N, Liu L, Zhao YO, Heisig J, Pan J, Eppler-Epstein R, Deponte K, Fish D, Fikrig E. 2014. Gut microbiota of the tick vector Ixodes scapularis modulate colonization of the Lyme disease spirochete Cell Host Microbe 15:58-71. http://dx.doi.org/10.1016/j.chom.2013.12.001.
20. Vaughn MF, Funkhouser SW, Lin FC, Fine J, Juliano JJ, Apperson CS, Meshnick SR. 2014. Long-lasting permethrin impregnated uniforms: a randomized-controlled trial for tick bite prevention. Am J Prev Med 46: 473-480. http://dx.doi.org/10.1016/j.amepre.2014.01.008.
21. Smith MP, Ponnusamy L, Jiang J, Ayyash LA, Richards AL, Apperson CS. 2010. Bacterial pathogens in Ixodid ticks from a Piedmont county in North Carolina: prevalence of rickettsial organisms. Vector Borne Zoonotic Dis 10:939-952. http://dx.doi.org/10.1089/vbz.2009.0178.
22. Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, Ursell LK, Lauber C, Zhou H, Song SJ, Huntley J, Ackermann GL, Berg-Lyons D, Holmes S, Caporaso JG, Knight R. 2013. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol 531:371-444. http://dx.doi.org/10.1016/B978-0-12-407863-5.00019-8.
23. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
24. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069-5072. http://dx.doi.org/10.1128/AEM.03006-05.
25. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610-618. http://dx.doi.org/10.1038/ismej.2011.139.
26. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. 2010. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266-267. http://dx.doi.org/10.1093/bioinformatics/btp636.
27. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. http://dx.doi.org/10.1371/journal.pone.0009490.
28. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
29. McMurdie PJ, Holmes S. 2014. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531. http: //dx.doi.org/10.1371/journal.pcbi.1003531.
30. Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228-8235. http://dx.doi.org/10.1128/AEM.71.12.8228-8235.2005.
31. Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. 2013. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2:16. http://dx.doi.org/10.1186/2047-217X-2-16.
32. Faith DP. 1992. Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1-10. http://dx.doi.org/10.1016/0006-3207(92)91201-3.
33. Knights D, Costello EK, Knight R. 2011. Supervised classification of human microbiota. FEMS Microbiol Rev 35:343-359. http://dx.doi.org /10.1111/j.1574-6976.2010.00251.x.
34. Zhang J, Kobert K, Flouri T, Stamatakis A. 2014. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614-620. http://dx.doi.org/10.1093/bioinformatics/btt593.
35. Parobek CM, Bailey JA, Hathaway NJ, Socheat D, Rogers WO, Juliano JJ. 2014. Differing patterns of selection and geospatial genetic diversity within two leading Plasmodium vivax candidate vaccine antigens. PLoS Negl Trop Dis 8:e2796. http://dx.doi.org/10.1371/journal.pntd.0002796.
36. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. 2004. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150:1741-1755. http://dx.doi.org/10.1099/mic.0.26944-0.
37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
38. Environmental Systems Resource Institute. 2013. ArcMap 10.2. Environmental Systems Resource Institute, Redlands, CA.
39. Zhang XC, Yang ZN, Lu B, Ma XF, Zhang CX, Xu HJ. 2014. The composition and transmission of microbiome in hard tick, Ixodes persulcatus, during blood meal. Ticks Tick-Borne Dis 5:864-870. http://dx.doi.org/10.1016/j.ttbdis.2014.07.009.
40. Telford SR, III. 2009. Status of the "East Side hypothesis" (transovarial interference) 25 years later. AnnNY Acad Sci 1166:144-150. http://dx.doi.org/10.1111/j.1749-6632.2009.04522.x.
41. Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE. 2003. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 40: 371-374. http://dx.doi.org/10.1603/0022-2585-40.3.371.
42. Kaaya GP, Okech MA. 1990. Microorganisms associated with tsetse in nature: preliminary resultsonisolation, identificationandpathogenicity. Int JTropInsect Sci 11:443-448. http://dx.doi.org/10.1017/S1742758400012868.
43. Pellegrini G, Levre E, Valentini P, Cadoni M. 1992. Cockroach infestation and possible contribution to the spread of some enterobacteria. Igiene Moderna 97:19-30.
44. Akinosoglou K, Perperis A, Siagris D, Goutou P, Spiliopoulou I, Gogos CA, Marangos M. 2012. Bacteraemia due to Cedecea davisae in a patient with sigmoid colon cancer: a case report and brief review of the literature. Diagn Microbiol Infect Dis 74:303-306. http://dx.doi.org/10.1016/j.diagmicrobio.2012.06.019.
45. Brinkerhoff RJ, Gilliam WF, Gaines D. 2014. Lyme disease, Virginia, USA, 2000-2011. Emerg Infect Dis 20:1661-1668. http://dx.doi.org/10.3201/eid2010.130782.
46. Weiss SJ, Xu Z, Amir A, Peddada S, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vazquez-Baeza Y, Birmingham A, Knight R. 2015. Effects of library size variance, sparsity, and compositionality on the analysis of microbiome data. PeerJ PrePrints 3:e1408. http://dx.doi.org/10.7287/peerj.preprints.1157v1.