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Microbiome analysis of the saliva and midgut from partially or fully engorged female adult Dermacentor silvarum ticks in China

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Abstract

Dermacentor silvarum is widely distributed in northern China and transmits several pathogens that cause diseases in humans and domestic animals. We analysed the comprehensive bacterial community of the saliva and midgut from partially and fully engorged female adult D. silvarum. Dermacentor silvarum samples were collected from Guyuan, China. Bacterial DNA was extracted from the saliva and midgut contents of partially or fully engorged female adult D. silvarum. Sequencing of the V3–V4 hypervariable regions of the 16S rRNA genes was performed using the IonS5TMXL platform. The bacterial diversity in saliva was higher than in the midgut. The bacterial diversity of saliva from fully engorged ticks was greater than in partially engorged tick saliva. The bacterial diversity in midguts from partially engorged ticks was greater than in fully engorged tick midguts. Proteobacteria was the most dominant bacterial phylum in all of the samples. Twenty-nine bacterial genera were detected in all of the samples. Rickettsia, Anaplasma, and Stenotrophomonas were the main genera. The symbionts Coxiella, Arsenophonus, and Wolbachia were also detected in all of the samples. Eight bacterial species were identified in all of the experimental samples. Anaplasma marginale was reported for the first time in D. silvarum.

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References

  • Battilani M, De Arcangeli S, Balboni A, Dondi F (2017) Genetic diversity and molecular epidemiology of Anaplasma. Infect Genet Evol 49:195–211

    Article  CAS  PubMed  Google Scholar 

  • Berrada ZL, Telford SR 3rd (2009) Burden of tick-borne infections on American companion animals. Top Companion Anim Med 24(4):175–181

    Article  PubMed  PubMed Central  Google Scholar 

  • Budachetri K, Browning RE, Adamson SW, Dowd SE, Chao CC, Ching WM, Karim S (2014) An insight into the microbiome of the Amblyomma maculatum (Acari: Ixodidae). J Med Entomol 51(1):119–129

    Article  CAS  PubMed  Google Scholar 

  • Budachetri K, Gaillard D, Williams J, Mukherjee N, Karim S (2016) A snapshot of the microbiome of Amblyomma tuberculatum ticks infesting the gopher tortoise, an endangered species. Ticks Tick Borne Dis 7(6):1225–1229

    Article  PubMed  PubMed Central  Google Scholar 

  • Budachetri K, Williams J, Mukherjee N, Sellers M, Moore F, Karim S (2017) The microbiome of neotropical ticks parasitizing on passerine migratory birds. Ticks Tick Borne Dis 8(1):170–173

    Article  PubMed  Google Scholar 

  • Cao WC, Zhan L, De Vlas SJ, Wen BH, Yang H, Richardus JH, Habbema JD (2008) Molecular detection of spotted fever group Rickettsia in Dermacentor silvarum from a forest area of northeastern China. J Med Entomol 45(4):741–744

    PubMed  Google Scholar 

  • Cao WC, Zhan L, He J, Foley JE, De Vlas SJ, Wu XM, Yang H, Richardus JH, Habbema JD (2006) Natural Anaplasma phagocytophilum infection of ticks and rodents from a forest area of Jilin Province, China. Am J Trop Med Hyg 75(4):664–668

    Article  CAS  PubMed  Google Scholar 

  • Chansang U, Mulla MS, Chantaroj S, Sawanpanyalert P (2010) The eye fly Siphunculina funicola (Diptera: Chloropidae) as a carrier of pathogenic bacteria in Thailand. Southeast Asian J Trop Med Public Health 41(1):61–71

    PubMed  Google Scholar 

  • Chen M, Fan MY, Bi DZ, Zhang JZ, Huang YP (1998) Detection of Rickettsia sibirica in ticks and small mammals collected in three different regions of China. Acta Virol 42(1):61–64

    CAS  PubMed  Google Scholar 

  • Chen Z, Yang X, Bu F, Yang X, Yang X, Liu J (2010) Ticks (acari: ixodoidea: argasidae, ixodidae) of China. Exp Appl Acarol 51(4):393–404

    Article  PubMed  Google Scholar 

  • Dahlgren FS, Mandel EJ, Krebs JW, Massung RF, McQuiston JH (2011) Increasing incidence of Ehrlichia chaffeensis and Anaplasma phagocytophilum in the United States, 2000–2007. Am J Trop Med Hyg 85(1):124–131

    Article  PubMed  PubMed Central  Google Scholar 

  • David MR, Santos LM, Vicente AC, Maciel-de-Freitas R (2016) Effects of environment, dietary regime and ageing on the dengue vector microbiota: evidence of a core microbiota throughout Aedes aegypti lifespan. Mem Inst Oswaldo Cruz 111(9):577–587

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng GP, Jiang ZJ (1991) Economic insect fauna of china. Science Press, Beijing in Chinese

    Google Scholar 

  • Duan D, Cheng T (2017) Determination of the microbial community features of Haemaphysalis flava in different developmental stages by high-throughput sequencing. J Basic Microbiol 57(4):302–308

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estrada-Pena A, Jongejan F (1999) Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23(9):685–715

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo S, Bonnin RA, Poirel L, Duranteau J, Nordmann P (2012) Identification of the naturally occurring genes encoding carbapenem-hydrolysing oxacillinases from Acinetobacter haemolyticus, Acinetobacter johnsonii, and Acinetobacter calcoaceticus. Clin Microbiol Infect 18(9):907–913

    Article  CAS  PubMed  Google Scholar 

  • Futse JE, Ueti MW, Knowles DP Jr, Palmer GH (2003) Transmission of Anaplasma marginale by Boophilus microplus: retention of vector competence in the absence of vector-pathogen interaction. J Clin Microbiol 41(8):3829–3834

    Article  PubMed  PubMed Central  Google Scholar 

  • Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, Brenner DJ (1991) Notes: Arsenophonus nasoniae gen. nov. sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol 41(4):563–565

    Article  Google Scholar 

  • Gong S, He B, Wang Z, Shang L, Wei F, Liu Q (2015) Tu C (2015) Nairobi sheep disease virus RNA in Ixodid ticks, China, 2013. Emerg Infect Dis 21(4):718–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorenflot A, Moubri K, Precigout E, Carcy B, Schetters TP (1998) Human babesiosis. Ann Trop Med Parasitol 92(4):489–501

    Article  CAS  PubMed  Google Scholar 

  • Guo DH, Zhang Y, Fu X, Gao Y, Liu YT, Qiu JH, Chang QC, Wang CR (2016) Complete mitochondrial genomes of Dermacentor silvarum and comparative analyses with another hard tick Dermacentor nitens. Exp Parasitol 169:22–27

    Article  CAS  PubMed  Google Scholar 

  • He X, Zhao J, Fu S, Yao L, Gao X, Liu Y, He Y, Liang G, Wang H (2018) Complete genomic characterization of three tick-borne encephalitis viruses detected along the China-North Korea border, 2011. Vector Borne Zoonotic Dis 18(10):554–559

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Igolkina Y, Rar V, Vysochina N, Ivanov L, Tikunov A, Pukhovskaya N, Epikhina T, Golovljova I, Tikunova N (2018) Genetic variability of Rickettsia spp. in Dermacentor and Haemaphysalis ticks from the Russian Far East. Ticks Tick Borne Dis 9(6):1594–1603

    Article  PubMed  Google Scholar 

  • Karim S, Budachetri K, Mukherjee N, Williams J, Kausar A, Hassan MJ, Adamson S, Dowd SE, Apanskevich D, Arijo A, Sindhu ZU, Kakar MA, Khan RMD, Ullah S, Sajid MS, Ali A, Iqbal Z (2017) A study of ticks and tick-borne livestock pathogens in Pakistan. PLoS Negl Trop Dis 11(6):e0005681

    Article  PubMed  PubMed Central  Google Scholar 

  • Keskin A, Bursali A, Snow DE, Dowd SE, Tekin S (2017) Assessment of bacterial diversity in Hyalomma aegyptium, H. marginatum and H. excavatum ticks through tag-encoded pyrosequencing. Exp Appl Acarol 73(3–4):461–475

    Article  CAS  PubMed  Google Scholar 

  • Khasnatinov MA, Liapunov AV, Manzarova EL, Kulakova NV, Petrova IV, Danchinova GA (2016) The diversity and prevalence of hard ticks attacking human hosts in Eastern Siberia (Russian Federation) with first description of invasion of non-endemic tick species. Parasitol Res 115(2):501–510

    Article  PubMed  Google Scholar 

  • Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E et al (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107(27):12168–12173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kocan KM, de la Fuente J, Guglielmone AA, Melendez RD (2003) Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev 16(4):698–712

    Article  PubMed  PubMed Central  Google Scholar 

  • Kose H, Karr TL (1995) Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech Dev 51(2–3):275–288

    Article  CAS  PubMed  Google Scholar 

  • Lalzar I, Harrus S, Mumcuoglu KS, Gottlieb Y (2012) Compsoition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl Environ Microbiol 78:4110–4116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Liu P, Wang C, Chen G, Kang M, Liu D, Li Z, He H, Dong Y, Zhang Y (2015) Serologic Evidence for Babesia bigemina Infection in Wild Yak (Bos Mutus) in Qinghai Province. China J Wildl Dis 51(4):872–875

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Li Q, Zhang X, Li Z, Wang Z, Song M, Wei F, Wang S, Liu Q (2016a) Characterization of rickettsiae in ticks in northeastern China. Parasit Vectors 9:498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu L, Li L, Liu J, Yu Z, Yang X, Liu J (2016b) Population dynamics of multiple symbionts in the hard tick, Dermacentor silvarum Olenev (Acari: Ixodidae). Ticks Tick Borne Dis 7(1):188–192

    Article  PubMed  Google Scholar 

  • Liu J, Liu Z, Zhang Y, Yang X, Gao Z (2005) Biology of Dermacentor silvarum (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 36(1–2):131–138

    Article  PubMed  Google Scholar 

  • Liu L, Li L, Liu J, Hu Y, Liu Z, Guo L, Liu J (2013) Coinfection of Dermacentor silvarum olenev (acari: ixodidae) by Coxiella-like, Arsenophonus-like, and Rickettsia-like symbionts. Appl Environ Microbiol 79(7):2450–2454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado-Ferreira E, Vizzoni VF, Piesman J, Gazeta GS, Soares CA (2015) Bacteria associated with Amblyomma cajennense tick eggs. Genet Mol Biol 38(4):477–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17(1):10–12

    Article  Google Scholar 

  • Merhej V, Angelakis E, Socolovschi C, Raoult D (2014) Genotyping, evolution and epidemiological findings of Rickettsia species. Infect Genet Evol 25:122–137

    Article  PubMed  Google Scholar 

  • Moraes AP, Videira SS, Bittencourt VR, Bittencourt AJ (2014) Antifungal activity of Stenotrophomonas maltophilia in Stomoxys calcitrans larvae. Rev Bras Parasitol 23(2):194–199

    Article  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  Google Scholar 

  • Moore ER, Krüger AS, Hauben L, Seal SE, Daniels MJ, De Baere R, De Wachter R, Timmis KN, Swings J (1997) 16S rRNA gene sequence analyses and inter- and intrageneric relationships of Xanthomonas species and Stenotrophomonas maltophilia. FEMS Microbiol Lett 151(2):145–153

    Article  CAS  PubMed  Google Scholar 

  • Murrell A, Dobson SJ, Yang X, Lacey E, Barker SC (2003) A survey of bacterial diversity in ticks, lice and fleas from Australia. Parasitol Res 89(4):326–334

    Article  PubMed  Google Scholar 

  • Okla H, Sosnowska M, Jasik KP, Slodki J, Wojtyczka RD (2012) Nonspecific Bacterial Flora Isolated from the Body Surface and Inside Ixodes ricinus Ticks. Pol J Microbiol 61(3):205–209

    Article  PubMed  Google Scholar 

  • Patton TG, Dietrich G, Brandt K, Dolan MC, Piesman J, Gilmore RD Jr (2012) Saliva, salivary gland, and hemolymph collection from Ixodes scapularis ticks. J Vis Exp 60:3894

    Google Scholar 

  • Pires ACAM, Villegas LEM, Campolina TB, Orfanó AS, Pimenta PFP, Secundino NFC (2017) Bacterial diversity of wild-caught Lutzomyia longipalpis (a vector of zoonotic visceral leishmaniasis in Brazil) under distinct physiological conditions by metagenomics analysis. Parasites Vectors 10(1):627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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. PLoS ONE 7(1):e30692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popov VL, Korenberg EI, Nefedova VV, Han VC, Wen JW, Kovalevskii YV, Gorelova NB, Walker DH (2007) Ultrastructural evidence of the ehrlichial developmental cycle in naturally infected Ixodes persulcatus ticks in the course of coinfection with Rickettsia, Borrelia, and a flavivirus. Vector Borne Zoonotic Dis 7(4):699–716

    Article  PubMed  Google Scholar 

  • Pukhovskaya NM, Morozova OV, Vysochina NP, Belozerova NB, Bakhmetyeva SV, Zdanovskaya NI, Seligman SJ, Ivanov LI (2018) Tick-borne encephalitis virus in arthropod vectors in the Far East of Russia. Ticks Tick Borne Dis 9(4):824–833

    Article  PubMed  Google Scholar 

  • Qiu Y, Nakao R, Ohnuma A, Kawamori F, Sugimoto C (2014) Microbial population analysis of the salivary glands of ticks; a possible strategy for the surveillance of bacterial pathogens. PLoS ONE 9(8):e103961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro JM (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 4(3):143–152

    CAS  PubMed  Google Scholar 

  • Santos AS, Bacellar F, Santos-Silva M, Formosinho P, Gracio AJ, Franca S (2002) Ultrastructural study of the infection process of Rickettsia conorii in the salivary glands of the vector tick Rhipicephalus sanguineus. Vector Borne Zoonotic Dis 2(3):165–177

    Article  CAS  PubMed  Google Scholar 

  • Smith TA, Driscoll T, Gillespie JJ, Raghavan R (2015) A Coxiella-like endosymbiont is a potential vitamin source for the Lone Star tick. Genome Biol Evol 7(3):831–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Xu R (2003) Ability of Ixodes persulcatus, Haemaphysalis concinna and Dermacentor silvarum ticks to acquire and transstadially transmit Borrelia garinii. Exp Appl Acarol 31(1–2):151–160

    Article  PubMed  Google Scholar 

  • Tian ZC, Liu GY, Shen H, Xie JR, Luo J, Tian MY (2012) First report on the occurrence of Rickettsia slovaca and Rickettsia raoultii in Dermacentor silvarum in China. Parasites Vectors 5:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turton JF, Shah J, Ozongwu C, Pike R (2010) Incidence of Acinetobacter species other than A. baumannii among clinical isolates of Acinetobacter: evidence for emerging species. J Clin Microbiol 48(4):1445–1449

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueti MW, Reagan JO Jr, Knowles DP Jr, Scoles GA, Shkap V, Palmer GH (2007) Identification of midgut and salivary glands as specific and distinct barriers to efficient tick-borne transmission of Anaplasma marginale. Infect Immun 75(6):2959–2964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vilcins IM, Old JM, Deane E (2009) Molecular detection of Rickettsia, Coxiella and Rickettsiella DNA in three native Australian tick species. Exp Appl Acarol 49(3):229–242

    Article  PubMed  Google Scholar 

  • Wang M, Zhu D, Dai J, Zhong Z, Zhang Y, Wang J (2018) Tissue localization and variation of major symbionts in Haemaphysalis longicornis, Rhipicephalus haemaphysaloides, and Dermacentor silvarum in China. Appl Environ Microbiol 84(10):1–37

    Article  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei F, Song M, Liu H, Wang B, Wang S, Wang Z, Ma H, Li Z, Zeng Z, Qian J, Liu Q (2016) Molecular detection and characterization of zoonotic and veterinary pathogens in ticks from Northeastern China. Front Microbiol 7:1913

    PubMed  PubMed Central  Google Scholar 

  • Wen B, Cao W, Pan H (2003) Ehrlichiae and ehrlichial diseases in China. Ann N Y Acad Sci 990:45–53

    Article  CAS  PubMed  Google Scholar 

  • Wen J, Jiao D, Wang JH, Yao DH, Liu ZX, Zhao G, Ju WD, Cheng C, Li YJ, Sun Y (2014) Rickettsia raoultii, the predominant Rickettsia found in Dermacentor silvarum ticks in China-Russia border areas. Exp Appl Acarol 63(4):579–585

    Article  PubMed  Google Scholar 

  • Wikel SK (1999) Tick modulation of host immunity: an important factor in pathogen transmission. Int J Parasitol 29(6):851–859

    Article  CAS  PubMed  Google Scholar 

  • Wolf A, Fritze A, Hagemann M, Berg G (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Microbiol 52(Pt 6):1937–1944

    CAS  PubMed  Google Scholar 

  • Yin H, Luo J (2007) Ticks of small ruminants in China. Parasitol Res 101(Suppl 2):S187–189

    Article  PubMed  Google Scholar 

  • Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, Zhang L, Zhang QF, Popov VL, Li C et al (2011) Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364(16):1523–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Liu W, Wu XM, Xin ZT, Zhao QM, Yang H, Cao WC (2008) Detection of Francisella tularensis in ticks and identification of their genotypes using multiple-locus variable-number tandem repeat analysis. BMC Microbiol 8:152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang L, Li S, Huang SJ, Wang ZD, Wei F, Feng XM, Jiang DX, Liu Q (2018) Isolation and genomic characterization of lymphocytic choriomeningitis virus in ticks from northeastern China. Transbound Emerg Dis 65(6):1733–1739

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Liu H, Xu B, Lu Q, Li L, Chang L, Zhang X, Fan D, Li G, Jin Y, Cui F, Shi Y, Li W, Xu J, Yu XJ (2012) Anaplasma phagocytophilum infection in domestic animals in ten provinces/cities of China. Am J Trop Med Hyg 87(1):185–189

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(6):864–870

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Funding

This research was financially supported by a grant from the National Science Foundation for Young Scientists of China (No. 31902294), the Youth Science Foundation of Hunan Agricultural University (No. 18QN24), the Natural Science Foundation of Hunan Province, China (No. 2018JJ2167), and the Double First-Class Construction Project of Hunan Agricultural University (No. SYL201802016).

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Duan, DY., Liu, GH. & Cheng, TY. Microbiome analysis of the saliva and midgut from partially or fully engorged female adult Dermacentor silvarum ticks in China. Exp Appl Acarol 80, 543–558 (2020). https://doi.org/10.1007/s10493-020-00478-2

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