Diversity analysis of the endosymbiotic bacterial community in field-collected Haemaphysalis ticks on the tropical Hainan Island, China
Language English Country Czech Republic Media electronic
Document type Journal Article
PubMed
37326358
DOI
10.14411/fp.2023.012
PII: 2023.012
Knihovny.cz E-resources
- Keywords
- 16S rRNA, Illumina MiSeq, bacterial community, endosymbiotic bacteria, tropics,
- MeSH
- Bacteria genetics MeSH
- Ixodidae * microbiology MeSH
- Ticks * MeSH
- Humans MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- China epidemiology MeSH
- Names of Substances
- RNA, Ribosomal, 16S MeSH
Ticks are important vectors of various pathogens that cause infectious diseases in humans. Endosymbiotic bacteria have been explored as targets for tick and tick-borne disease control. However, the tick bacterial community on Hainan Island, which is the largest tropical island in China and has an environment favourable to ticks, has not yet been studied. In this study, we surveyed the bacterial community of ticks collected from grass in one village in Haikou. A total of 20 ticks were morphologically and molecularly identified as Haemaphysalis spp. The tick bacterial 16S rRNA hypervariable region amplicon libraries were sequenced on an Illumina MiSeq platform. A total of 10 possible bacterial genera were detected, indicating a low-diversity bacterial community profile. The dominant bacterial genus, Massilia, accounted for 97.85% of the population. Some other bacterial genera, including Arsenophonus and Pseudomonas, have been reported to play a role in tick development and tick-borne pathogen transmission in other tick species. Overall, the study highlights the first descriptive understanding of the tick bacterial community on Hainan Island and provides a basis for deciphering the interactions between the tick microbiome and tick-borne pathogens.
See more in PubMed
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990: Basic local alignment search tool. J. Mol. Biol. 215: 403-410. PubMed DOI
Atre N.M., Alagarasu K., Shil P. 2022: ArVirInd-a database of arboviral antigenic proteins from the Indian subcontinent. PeerJ 10: e13851. PubMed DOI
Bolger A.M., Lohse M., Usadel B. 2014: Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120. PubMed DOI
Boulanger N., Boyer P., Talagrand-Reboul E., Hansmann Y. 2019: Ticks and tick-borne diseases. Med. Mal. Infect. 49: 87-97. PubMed DOI
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: 170-173. PubMed DOI
Cafarchia C., Pellegrino R., Romano V., Friuli M., Demitri C., Pombi M., Benelli G., Otranto D. 2022: Delivery and effectiveness of entomopathogenic fungi for mosquito and tick control: current knowledge and research challenges. Acta Trop. 234: 106627. PubMed DOI
Campelo Morillo R.A., Tong X., Xie W., Abel S., Orchard L.M., Daher W., Patel D.J., Llinás M., Le Roch K.G., Kafsack B.F.C. 2022: The transcriptional regulator HDP1 controls expansion of the inner membrane complex during early sexual differentiation of malaria parasites. Nat. Microbiol. 7: 289-299. PubMed DOI
Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., McDonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. 2010: QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336. PubMed DOI
Chavatte J. M., Octavia S. 2021: The complete mitochondrial genome of Dermacentor (Indocentor) auratus (Acari, Ixodidae). Parasite 28: 6. PubMed DOI
Cheng G., Liu Y., Wang P., Xiao X. 2016: Mosquito defense strategies against viral infection. Trends Parasitol. 32: 177-186. PubMed DOI
Chicana B., Couper L.I., Kwan J.Y., Tahiraj E., Swei A. 2019: Comparative microbiome profiles of sympatric tick species from the Far-Western United States. Insects 10: 353. PubMed DOI
Couper L.I., Kwan J.Y., Ma J., Swei A. 2019: Drivers and patterns of microbial community assembly in a Lyme disease vector. Ecol. Evol. 9: 7768-7779. PubMed DOI
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: 302-308. PubMed DOI
Edgar R.C., Haas B.J., Clemente J.C., Quince C., Knight R. 2011: UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200. PubMed DOI
Engel P., Moran N.A. 2013: The gut microbiota of insects - diversity in structure and function. FEMS Microbiol. Rev. 37: 699-735. PubMed DOI
Fogaça A.C., Sousa G., Pavanelo D.B., Esteves E., Martins L.A., Urbanová V., Kopáček P., Daffre S. 2021: Tick immune system: what is known, the interconnections, the gaps, and the challenges. Front. Immunol. 12: 628054. PubMed DOI
Fosso B., Pesole G., Rosselló F., Valiente G. 2018: Unbiased taxonomic annotation of metagenomic samples. J. Comput. Biol. 25: 348-360. PubMed DOI
Galay R.L., Manalo A.A.L., Dolores S.L.D., Aguilar I.P.M., Sandalo K.A.C., Cruz K.B., Divina B.P., Andoh M., Masatani T., Tanaka T. 2018: Molecular detection of tick-borne pathogens in canine population and Rhipicephalus sanguineus (sensu lato) ticks from southern Metro Manila and Laguna, Philippines. Parasit. Vectors 11: 643. PubMed DOI
Gu X., Yu Z., Yang G., Sun J., Wei H., Li K., Wang S. 2010: [Genetic relationship and sequence variation of Haemaphysalis longicornis and H. conicinna based on ITS-2, COⅠ and COⅡ gene sequences.] Chin. J. Anim. Vet. Sci. 41: 746-754. (In Chinese.)
Gurfield N., Grewal S., Cua L.S., Torres P.J., Kelley S.T. 2017: Endosymbiont interference and microbial diversity of the Pacific coast tick, Dermacentor occidentalis, in San Diego County, California. PeerJ 5: e3202. PubMed DOI
Jiang J.F., Jiang B.G., Yu J.H., Zhang W.Y., Gao H.W., Zhan L., Sun Y., Zhang X.A., Zhang P.H., Liu W., Wu X.M., Xu R.M., Cao W.C. 2011: Anaplasma phagocytophilum infection in ticks, China-Russia border. Emerg. Infect. Dis. 17: 932-934. PubMed DOI
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. PubMed DOI
Kämpfer P., Lodders N., Martin K., Falsen E. 2012: Massilia oculi sp. nov., isolated from a human clinical specimen. Int. J. Syst. Evol. Microbiol. 62: 364-369. PubMed DOI
Kohls G.M. 1957: Tick (Ixodoidae) of Borneo and Malaya. Stud. Inst. Med. Res. Malaya 28: 65-94.
La Scola B., Birtles R.J., Mallet M.N., Raoult D. 1998: Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. J. Clin. Microbiol. 36: 2847-2852. PubMed DOI
Li A.Z., Han X.B., Zhang M.X., Zhou Y., Chen M., Yao Q., Zhu H.H. 2019: culture-dependent and -independent analyses reveal the diversity, structure, and assembly mechanism of benthic bacterial community in the Ross Sea, Antarctica. Front. Microbiol. 10: 2523. PubMed DOI
Luo L.M., Zhao L., Wen H.L., Zhang Z.T., Liu J.W., Fang L.Z., Xue Z.F., Ma D.Q., Zhang X.S., Ding S.J., Lei X.Y., Yu X.J. 2015: Haemaphysalis longicornis ticks as reservoir and vector of severe fever with thrombocytopenia syndrome virus in China. Emerg. Infect. Dis. 21: 1770-1776. PubMed DOI
Madden T.L., Tatusov R.L., Zhang J. 1996: Applications of network BLAST server. Methods Enzymol. 266: 131-141. PubMed DOI
Magoč T., Salzberg S.L. 2011: FLASH: Fast Length Adjustment of Short reads to improve genome assemblies. Bioinformatics 27: 2957-2963. PubMed DOI
Mansfield K.L., Jizhou L., Phipps L.P., Johnson N. 2017: Emerging tick-borne viruses in the twenty-first century. Front. Cell Infect. Microbiol. 7: 298. PubMed DOI
Narasimhan S., Fikrig E. 2015: Tick microbiome: the force within. Trends Parasitol. 31: 315-323. PubMed DOI
Narasimhan S., Swei A., Abouneameh S., Pal U., Pedra J.H.F., Fikrig E. 2021: Grappling with the tick microbiome. Trends Parasitol. 37: 722-733. PubMed DOI
Nazipi S., Elberg C. L., Busck M. M., Lund M. B., Bilde T., Schramm A. 2021: The bacterial and fungal nest microbiomes in populations of the social spider Stegodyphus dumicola. Syst. Appl. Microbiol. 44: 126222. PubMed DOI
Pichler M., Coskun Ö K., Ortega-Arbulú A.S., Conci N., Wörheide G., Vargas S., Orsi W.D. 2018: A 16S rRNA gene sequencing and analysis protocol for the Illumina MiniSeq platform. Microbiologyopen 7: e00611. PubMed DOI
Rodríguez-Ruano S.M., Juhaňáková E., Vávra J., Nováková E. 2020: Methodological insight into mosquito microbiome studies. Front. Cell Infect. Microbiol. 10: 86. PubMed DOI
Ross B.D., Hayes B., Radey M.C., Lee X., Josek T., Bjork J., Neitzel D., Paskewitz S., Chou S., Mougous J.D. 2018: Ixodes scapularis does not harbor a stable midgut microbiome. ISME J. 12: 2596-2607. PubMed DOI
Stanley H.M., Ford S.L., Snellgrove A.N., Hartzer K., Smith E.B., Krapiunaya I., Levin M.L. 2020: The ability of the invasive Asian longhorned tick Haemaphysalis longicornis (Acari: Ixodidae) to acquire and transmit Rickettsia rickettsii (Rickettsiales: Rickettsiaceae), the agent of Rocky Mountain spotted fever, under laboratory conditions. J. Med. Entomol. 57: 1635-1639. PubMed DOI
Tamura K., Stecher G., Kumar S. 2021: MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol. Biol. Evol. 38: 3022-3027. PubMed DOI
Tan S. C., Chong C. W., Yap I. K. S., Thong K. L., Teh C. S. J. 2020: Comparative assessment of faecal microbial composition and metabonome of swine, farmers and human control. Sci. Rep. 10: 8997. PubMed DOI
Thapa S., Zhang Y., Allen M. S. 2019: Bacterial microbiomes of Ixodes scapularis ticks collected from Massachusetts and Texas, USA. BMC Microbiol. 19: 138. PubMed DOI
Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. 2016: W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44: W232-W235. PubMed DOI
Tufa T.B., Wölfel S., Zubriková D., Víchová B., Andersson M., Rieß R., Rutaihwa L., Fuchs A., Orth H.M., Häussinger D., Feldt T., Poppert S., Dobler G., Bakkes D.K., Chitimia-Dobler L. 2021: Tick species from cattle in the Adama Region of Ethiopia and pathogens detected. Exp. Appl. Acarol. 84: 459-471. PubMed DOI
Tyurin M., Kabilov M.R., Smirnova N., Tomilova O.G., Yaroslavtseva O., Alikina T., Glupov V.V., Kryukov V.Y. 2021: Can potato plants be colonized with the fungi Metarhizium and Beauveria under their natural load in agrosystems? Microorganisms 9: 1373. PubMed DOI
Van Eesbeeck V., Props R., Mysara M., Petit P.C.M., Rivasseau C., Armengaud J., Monsieurs P., Mahillon J., Leys N. 2021: Cyclical patterns affect microbial dynamics in the water basin of a nuclear research reactor. Front. Microbiol. 12: 744115. PubMed DOI
Verbanic S., Shen Y., Lee J., Deacon J.M., Chen I.A. 2020: Microbial predictors of healing and short-term effect of debridement on the microbiome of chronic wounds. NPJ Biofilms Microbiomes 6: 21. PubMed DOI
Walker A., Bouattour A., Camicas J.L., Estrada-Peña A., Horak I.G., Latif A.A., Pegram R.G. and Preston P.M. 2003: Speciec of Haemaphysalis leachi, H. punctata and H. sulcata. In: Ticks of Domestic Animals in Africa: A Guide to Identifi-cation of Species. Bioscience Reports, Edinburgh, pp. 77-85.
Weinroth M.D., Belk A.D., Dean C., Noyes N., Dittoe D.K., Rothrock M.J., Ricke S.C., Myer P.R., Henniger M.T., Ramírez G.A., Oakley B.B., Summers K. L., Miles A.M., Ault-Seay T.B., Yu Z., Metcalf J.L., Wells J.E. 2022: Considerations and best practices in animal science 16S ribosomal RNA gene sequencing microbiome studies. J. Anim. Sci. 100: skab346. PubMed DOI
Wikel S.K. 2018: Ticks and tick-borne infections: complex ecology, agents, and host interactions. Vet. Sci. 5: 60. PubMed DOI
Wikel S.K. 2021: Immunobiology of tick-host-pathogen interactions. Parasite Immunol. 43: e12818. PubMed DOI
Yuan C., Wu J., Peng Y., Li Y., Shen S., Deng F., Hu Z., Zhou J., Wang M., Zou Z. 2020: Transcriptome analysis of the innate immune system of Hyalomma asiaticum. J. Invertebr. Pathol. 177: 107481. PubMed DOI
Yuan C., Xing L., Wang M., Hu Z., Zou Z. 2021: Microbiota modulates gut immunity and promotes baculovirus infection in Helicoverpa armigera. Insect Sci. 28: 1766-1779. PubMed DOI
Yuan C., Xing L., Wang M., Wang X., Yin M., Wang Q., Hu Z., Zou Z. 2017: Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PLoS Pathog. 13: e1006645. PubMed DOI
Zhang R., Huang Z., Yu G., Zhang Z. 2019: Characterization of microbiota diversity of field-collected Haemaphysalis longicornis (Acari: Ixodidae) with regard to sex and blood meals. J. Basic Microbiol. 59: 215-223. PubMed DOI
Zhuang L., Sun Y., Cui X.M., Tang F., Hu J.G., Wang L.Y., Cui N., Yang Z.D., Huang D.D., Zhang X.A., Liu W., Cao W.C. 2018: Transmission of severe fever with thrombocytopenia syndrome virus by Haemaphysalis longicornis Ticks, China. Emerg. Infect. Dis. 24: 868-871. PubMed DOI