Bacterial microbiomes of Ixodes scapularis ticks collected from Massachusetts and Texas, USA

Santosh Thapa1, Yan Zhang1, Michael S. Allen1
1Tick Borne Disease Research Laboratory, Department of Microbiology, Immunology and Genetics, University of North Texas Health Science Center, Fort Worth, TX, USA

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Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129(Suppl):S3–14.

Yuan DT. A metagenomic study of the tick midgut. Thesis (MS). Houston: The University of Texas; 2010.

Adrion ER, Aucott J, Lemke KW, Weiner JP. Health care costs, utilization and patterns of care following Lyme disease. PLoS One. 2015;10(2):e0116767.

Narasimhan S, Fikrig E. Tick microbiome: the force within. Trends Parasitol. 2015;31(7):315–23.

Zhang X, Meltzer MI, Pena CA, Hopkins AB, Wroth L, Fix AD. Economic impact of Lyme disease. Emerg Infect Dis. 2006;12(4):653–60.

Clay K, Fuqua C. The tick microbiome: diversity, distribution and influence of the internal microbial community for a blood-feeding disease vector. In: Workshop report: 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, DC: National Academies Press; 2010. p. A193–214.

Rochon K, Scoles GA, Lysyk TJ. Dispersion and sampling of adult Dermacentor andersoni in rangeland in Western North America. J Med Entomol. 2012;49(2):253–61.

Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP. Lyme disease-a tick-borne spirochetosis. Science (New York, NY). 1982;216(4552):1317–9.

Eisen RJ, Eisen L, Beard CB. County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. J Med Entomol. 2016;53(2):349–86.

Piesman J, Eisen L. Prevention of tick-borne diseases. Annu Rev Entomol. 2008;53:323–43.

Ebel GD. Update on Powassan virus: emergence of a north American tick-borne flavivirus. Annu Rev Entomol. 2010;55:95–110.

Prusinski MA, Kokas JE, Hukey KT, Kogut SJ, Lee J, Backenson PB. 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. 2014;51(1):226–36.

Spielman A, Clifford CM, Piesman J, Corwin MD. Human babesiosis on Nantucket Island, USA: description of the vector, Ixodes (Ixodes) dammini, n. sp. (Acarina: Ixodidae). J Med Entomol. 1979;15(3):218–34.

Scoles GA, Papero M, Beati L, Fish D. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis. 2001;1(1):21–34.

Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, Fish D, Krause PJ. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis. 2011;17(10):1816–23.

Krause PJ, Narasimhan S, Wormser GP, Rollend L, Fikrig E, Lepore T, Barbour A, Fish D. Human Borrelia miyamotoi infection in the United States. N Engl J Med. 2013;368(3):291–3.

Hinckley AF, Connally NP, Meek JI, Johnson BJ, Kemperman MM, Feldman KA, White JL, Mead PS. Lyme disease testing by large commercial laboratories in the United States. Clin Infect Dis. 2014;59(5):676–81.

Nelson CA, Saha S, Kugeler KJ, Delorey MJ, Shankar MB, Hinckley AF, Mead PS. Incidence of clinician-diagnosed Lyme disease, United States, 2005-2010. Emerg Infect Dis. 2015;21(9):1625–31.

Lyme disease: data and statistics. [ https://www.cdc.gov/lyme/stats/index.html ]. Accessed 17 Dec 2017.

Xu G, Mather TN, Hollingsworth CS, Rich SM. Passive surveillance of Ixodes scapularis (say), their biting activity, and associated pathogens in Massachusetts. Vector Borne Zoonotic Dis. 2016;16(8):520–7.

Adelson ME, Rao RV, Tilton RC, Cabets K, Eskow E, Fein L, Occi JL, Mordechai E. Prevalence of Borrelia burgdorferi, Bartonella spp., Babesia microti, and Anaplasma phagocytophila in Ixodes scapularis ticks collected in northern New Jersey. J Clin Microbiol. 2004;42(6):2799–801.

Moreno CX, Moy F, Daniels TJ, Godfrey HP, Cabello FC. Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess counties, New York. Environ Microbiol. 2006;8(5):761–72.

Eisen L, Eisen RJ, Mun J, Salkeld DJ, Lane RS. Transmission cycles of Borrelia burgdorferi and B. bissettii in relation to habitat type in northwestern California. J Vector Ecol. 2009;34(1):81–91.

Clark KL, Oliver JH Jr, James AM, Durden LA, Banks CW. Prevalence of Borrelia burgdorferi sensu lato infection among rodents and host-seeking ticks in South Carolina. J Med Entomol. 2002;39(1):198–206.

Maggi RG, Reichelt S, Toliver M, Engber B. Borrelia species in Ixodes affinis and Ixodes scapularis ticks collected from the coastal plain of North Carolina. Ticks Tick-Borne Dis. 2010;1(4):168–71.

Kiersten JK, Grace MF, Joseph DF, Paul SM. Geographic distribution and expansion of human Lyme disease, United States. Emerg Infect Dis. 2015;21(8):1455.

Estrada-Pena A, Ayllon N, de la Fuente J. Impact of climate trends on tick-borne pathogen transmission. Front Physiol. 2012;3:64.

Monaghan AJ, Moore SM, Sampson KM, Beard CB, Eisen RJ. Climate change influences on the annual onset of Lyme disease in the United States. Ticks Tick-Borne Dis. 2015;6(5):615–22.

Ostfeld RS, Brunner JL. Climate change and Ixodes tick-borne diseases of humans. Philos Trans R Soc Lond Ser B Biol Sci. 2015;370(1665):20140051.

Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, Cortinas R, Vourc'h G, Melton F, Hickling GJ, et al. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. Am J Trop Med Hyg. 2012;86(2):320–7.

Kelly RR, Gaines D, Gilliam WF, Brinkerhoff RJ. Population genetic structure of the Lyme disease vector Ixodes scapularis at an apparent spatial expansion front. Infect Genetics Evol. 2014;27:543–50.

Arsnoe IM, Hickling GJ, Ginsberg HS, McElreath R, Tsao JI. Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human Lyme disease risk. PLoS One. 2015;10(5):e0127450.

Spielman A, Wilson ML, Levine JF, Piesman J. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annu Rev Entomol. 1985;30:439–60.

Eisen RJ, Eisen L, Ogden NH, Beard CB. Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and Lyme disease in North America. J Med Entomol. 2016;53(2):250–61.

Ahantarig A, Trinachartvanit W, Baimai V, Grubhoffer L. Hard ticks and their bacterial endosymbionts (or would be pathogens). Folia Microbiol. 2013;58(5):419–28.

Gall CA, Reif KE, Scoles GA, Mason KL, Mousel M, Noh SM, Brayton KA. The bacterial microbiome of Dermacentor andersoni ticks influences pathogen susceptibility. ISME J. 2016;10(8):1846–55.

Smith TA, Driscoll T, Gillespie JJ, Raghavan R. A Coxiella-like endosymbiont is a potential vitamin source for the lone star tick. Genome Biol Evol. 2015;7(3):831–8.

Zhong J, Jasinskas A, Barbour AG. Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS One. 2007;2(5):e405.

Swei A, Kwan JY. Tick microbiome and pathogen acquisition altered by host blood meal. ISME J. 2017;11(3):813–6.

Clow KM, Weese JS, Rousseau J, Jardine CM. Microbiota of field-collected Ixodes scapularis and Dermacentor variabilis from eastern and southern Ontario, Canada. Ticks Tick-Borne Dis. 2018;9(2):235–44.

Zolnik CP, Prill RJ, Falco RC, Daniels TJ, Kolokotronis SO. Microbiome changes through ontogeny of a tick pathogen vector. Mol Ecol. 2016;25(19):4963–77.

Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, Hastriter MW, Nelson DE, Rong R, Munro D, Dong Q, et al. The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J. 2012;7:221.

Rynkiewicz EC, Hemmerich C, Rusch DB, Fuqua C, Clay K. Concordance of bacterial communities of two tick species and blood of their shared rodent host. Mol Ecol. 2015;24(10):2566–79.

Van Treuren W, Ponnusamy L, Brinkerhoff RJ, Gonzalez A, Parobek CM, Juliano JJ, Andreadis TG, Falco RC, Ziegler LB, Hathaway N, et al. Variation in the microbiota of Ixodes ticks with regard to geography, species, and sex. Appl Environ Microbiol. 2015;81(18):6200–9.

Thapa S, Zhang Y, Allen MS. Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks. MicrobiologyOpen. 2018;8(5):e00719.

Kurtti TJ, Felsheim RF, Burkhardt NY, Oliver JD, Heu CC, Munderloh UG. Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis. Int J Syst Evol Microbiol. 2015;65(Pt 3):965–70.

Shade A. Diversity is the question, not the answer. ISME J. 2016;11(1):1–6.

Hunter DJ, Torkelson JL, Bodnar J, Mortazavi B, Laurent T, Deason J, Thephavongsa K, Zhong J. The Rickettsia endosymbiont of Ixodes pacificus contains all the genes of de novo folate biosynthesis. PLoS One. 2015;10(12):e0144552.

Azad AF, Beard CB. Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis. 1998;4(2):179–86.

Paddock CD, Sumner JW, Comer JA, Zaki SR, Goldsmith CS, Goddard J, McLellan SL, Tamminga CL, Ohl CA. Rickettsia parkeri: a newly recognized cause of spotted fever rickettsiosis in the United States. Clin Infect Dis. 2004;38(6):805–11.

Noda H, Munderloh UG, Kurtti TJ. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol. 1997;63(10):3926–32.

Budachetri K, Browning RE, Adamson SW, Dowd SE, Chao C-C, Ching W-M, Karim S. An insight into the microbiome of the Amblyomma maculatum (Acari: Ixodidae). J Med Entomol. 2014;51(1):119–29.

Cape Cod deer tick project [ https://www.cranberries.org/sites/default/files/uploads/pdf/Meeting_files/DeerTicks_LarryDapsis.pdf ]. Accessed 3 Apr 2018.

Trout Fryxell RT, DeBruyn JM. The microbiome of Ehrlichia-infected and uninfected lone star ticks (Amblyomma americanum). PLoS One. 2016;11(1):e0146651.

Mousson L, Martin E, Zouache K, Madec Y, Mavingui P, Failloux AB. Wolbachia modulates chikungunya replication in Aedes albopictus. Mol Ecol. 2010;19(9):1953–64.

Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 2010;6(4):e1000833.

Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, Hurst GD. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 2008;6(1):27.

Hartelt K, Oehme R, Frank H, Brockmann SO, Hassler D, Kimmig P. 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. 2004;293(Suppl 37):86–92.

Plantard O, Bouju-Albert A, Malard MA, Hermouet A, Capron G, Verheyden H. Detection of Wolbachia in the tick Ixodes ricinus is due to the presence of the hymenoptera endoparasitoid Ixodiphagus hookeri. PLoS One. 2012;7(1):e30692.

Benson MJ, Gawronski JD, Eveleigh DE, Benson DR. Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol. 2004;70(1):616–20.

Menchaca AC, Visi DK, Strey OF, Teel PD, Kalinowski K, Allen MS, Williamson PC. Preliminary assessment of microbiome changes following blood-feeding and survivorship in the Amblyomma americanum nymph-to-adult transition using semiconductor sequencing. PLoS One. 2013;8(6):e67129.

WCt B, Piesman J. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci U S A. 1994;91(21):10034–8.

16S Illumina amplicon protocol [ http://press.igsb.anl.gov/earthmicrobiome/protocols-and-standards/16s/ ]. Accessed 15 Apr 2017.

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41.

Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96.

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200.

Schloss PD, Westcott SL. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol. 2011;77(10):3219–26.

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72.

McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012;6(3):610–8.

Hill TC, Walsh KA, Harris JA, Moffett BF. Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol. 2003;43(1):1–11.

Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57(1):289–300.

Benjamini Y. Discovering the false discovery rate. J R Stat Soc. 2010;72(4):405–16.

Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome. 2017;5(1):27.