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Cell
09 03, 2020;182 (5): 1328-1340.e13.

Large-Scale Comparative Analyses of Tick Genomes Elucidate Their Genetic Diversity and Vector Capacities.

Na Jia, Jinfeng Wang, Wenqiang Shi, Lifeng Du, Yi Sun, Wei Zhan, Jia-Fu Jiang, Qian Wang, Bing Zhang, Peifeng Ji, Lesley Bell-Sakyi, Xiao-Ming Cui, Ting-Ting Yuan, Bao-Gui Jiang, Wei-Fei Yang, Tommy Tsan-Yuk Lam, Qiao-Cheng Chang, Shu-Jun Ding, Xian-Jun Wang, Jin-Guo Zhu, Xiang-Dong Ruan, Lin Zhao, Jia-Te Wei, Run-Ze Ye, Teng Cheng Que, Chun-Hong Du, Yu-Hao Zhou, Jing Xia Cheng, Pei-Fang Dai, Wen-Bin Guo, Xiao-Hu Han, En-Jiong Huang, Lian-Feng Li, Wei Wei, Yu-Chi Gao, Jing-Ze Liu, Hong-Ze Shao, Xin Wang, Chong-Cai Wang, Tian-Ci Yang, Qiu-Bo Huo, Wei Li, Hai-Ying Chen, Shen-En Chen, Ling-Guo Zhou, Xue-Bing Ni, Jun-Hua Tian, Yue Sheng, Tao Liu, Yu-Sheng Pan, Luo-Yuan Xia, Jie Li, Tick Genome and Microbiome Consortium (TIGMIC), Fangqing Zhao, Wu-Chun Cao
Author Information
  1. Na Jia: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Research Unit of Discovery and Tracing of Natural Focus Diseases, Chinese Academy of Medical Sciences, Beijing 100071, P.R. China.
  2. Jinfeng Wang: Computational Genomics Lab, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P.R. China.
  3. Wenqiang Shi: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  4. Lifeng Du: Computational Genomics Lab, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China.
  5. Yi Sun: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  6. Wei Zhan: Annoroad Gene Technology (Beijing) Company Limited, Beijing 100176, P.R. China.
  7. Jia-Fu Jiang: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Research Unit of Discovery and Tracing of Natural Focus Diseases, Chinese Academy of Medical Sciences, Beijing 100071, P.R. China.
  8. Qian Wang: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China.
  9. Bing Zhang: Computational Genomics Lab, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China.
  10. Peifeng Ji: Computational Genomics Lab, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China.
  11. Lesley Bell-Sakyi: Department of Infection Biology and Microbiomes, Institute of Infection, Ecological and Veterinary Sciences, University of Liverpool, Liverpool L3 5RF, UK.
  12. Xiao-Ming Cui: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Research Unit of Discovery and Tracing of Natural Focus Diseases, Chinese Academy of Medical Sciences, Beijing 100071, P.R. China.
  13. Ting-Ting Yuan: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  14. Bao-Gui Jiang: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  15. Wei-Fei Yang: Annoroad Gene Technology (Beijing) Company Limited, Beijing 100176, P.R. China.
  16. Tommy Tsan-Yuk Lam: State Key Laboratory of Emerging Infectious Diseases and Centre of Influenza Research, School of Public Health, The University of Hong Kong, Hong Kong SAR, China.
  17. Qiao-Cheng Chang: College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang, P.R. China.
  18. Shu-Jun Ding: Shandong Center for Disease Control and Prevention, Shandong Provincial Key Laboratory of Communicable Disease Control and Prevention, Jinan 250014, Shandong, P.R. China.
  19. Xian-Jun Wang: Shandong Center for Disease Control and Prevention, Shandong Provincial Key Laboratory of Communicable Disease Control and Prevention, Jinan 250014, Shandong, P.R. China.
  20. Jin-Guo Zhu: ManZhouLi Customs District, Manzhouli 021400, Inner Mongolia, P.R. China.
  21. Xiang-Dong Ruan: Academy of Forest Inventory and Planning, State Forestry and Grassland Administration, Beijing 100714, P.R. China.
  22. Lin Zhao: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China.
  23. Jia-Te Wei: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China.
  24. Run-Ze Ye: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China.
  25. Teng Cheng Que: Guangxi Zhuang Autonomous Region Terrestrial Wildlife Medical-aid and Monitoring Epidemic Diseases Research Center, Nanjing 530028, Guangxi, P.R. China.
  26. Chun-Hong Du: Yunnan Institute for Endemic Diseases Control and Prevention, Dali 671000, Yunnan, P.R. China.
  27. Yu-Hao Zhou: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  28. Jing Xia Cheng: Shanxi Provence Center for Disease Control and Prevention, Xian 030012, Shanxi, P.R. China.
  29. Pei-Fang Dai: Shanxi Provence Center for Disease Control and Prevention, Xian 030012, Shanxi, P.R. China.
  30. Wen-Bin Guo: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  31. Xiao-Hu Han: Shenyang Agriculture University, Shenyang 110866, Liaoning, P.R. China.
  32. En-Jiong Huang: Fuzhou International Travel Healthcare Center, Fuzhou 350001, Fujian, P.R. China.
  33. Lian-Feng Li: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  34. Wei Wei: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  35. Yu-Chi Gao: Annoroad Gene Technology (Beijing) Company Limited, Beijing 100176, P.R. China.
  36. Jing-Ze Liu: Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, Hebei, P.R. China.
  37. Hong-Ze Shao: Animal Husbandry and Veterinary Science Research Institute of Jilin Province, Changchun 130062, Jilin, P.R. China.
  38. Xin Wang: Qingjiangpu District Center for Disease Control and Prevention, Huai'an 223001, Jiangsu, P.R. China.
  39. Chong-Cai Wang: Hainan International Travel Healthcare Center, Haikou 570311, Hainan, P.R. China.
  40. Tian-Ci Yang: State Key Lab of Mosquito-borne Diseases, Hangzhou International Tourism Healthcare Center, Hangzhou Customs of China, Hangzhou 310012, Zhejiang, P.R. China.
  41. Qiu-Bo Huo: Mudanjiang Forestry Central Hospital, Mudanjiang 157000, Heilongjiang, P.R. China.
  42. Wei Li: Xinjiang Center for Disease Control and Prevention, Urumqi 830002, Xinjiang, P.R. China.
  43. Hai-Ying Chen: Collaboration Unit for Field Epidemiology of the State Key Laboratory for Infectious Disease Prevention and Control, Nanchang Center for Disease Control and Prevention. Nanchang 330038, Jiangxi, P.R. China.
  44. Shen-En Chen: Collaboration Unit for Field Epidemiology of the State Key Laboratory for Infectious Disease Prevention and Control, Nanchang Center for Disease Control and Prevention. Nanchang 330038, Jiangxi, P.R. China.
  45. Ling-Guo Zhou: Shaanxi Natural Reserve and Wildlife Administration Station, Xi'an 710082, Shaanxi, P.R. China.
  46. Xue-Bing Ni: State Key Laboratory of Emerging Infectious Diseases and Centre of Influenza Research, School of Public Health, The University of Hong Kong, Hong Kong SAR, China.
  47. Jun-Hua Tian: Wuhan Center for Disease Control and Prevention, Wuhan 430015, Hubei, P.R. China.
  48. Yue Sheng: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  49. Tao Liu: Annoroad Gene Technology (Beijing) Company Limited, Beijing 100176, P.R. China.
  50. Yu-Sheng Pan: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  51. Luo-Yuan Xia: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  52. Jie Li: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China.
  53. Fangqing Zhao: Computational Genomics Lab, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P.R. China; Research Unit of Discovery and Tracing of Natural Focus Diseases, Chinese Academy of Medical Sciences, Beijing 100071, P.R. China; Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, Yunan, P.R. China; Key Laboratory of Systems Biology, Hangzhou Institute for Advanced Study, University of the Chinese Academy of Sciences, Chinese Academy of Sciences, Hangzhou, Zhejiang, P.R. China; University of the Chinese Academy of Sciences, Beijing 100049, P.R. China. Electronic address: zhfq@biols.ac.cn.
  54. Wu-Chun Cao: State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China; Institute of EcoHealth, School of Public Health, Shandong University, 44 Wenhuaxi Street, Jinan 250012, Shandong, P.R. China; Research Unit of Discovery and Tracing of Natural Focus Diseases, Chinese Academy of Medical Sciences, Beijing 100071, P.R. China. Electronic address: caowc@bmi.ac.cn.
PMID: 32814014 DOI: 10.1016/j.cell.2020.07.023

Abstract

Among arthropod vectors, ticks transmit the most diverse human and animal pathogens, leading to an increasing number of new challenges worldwide. Here we sequenced and assembled high-quality genomes of six ixodid tick species and further resequenced 678 tick specimens to understand three key aspects of ticks: genetic diversity, population structure, and pathogen distribution. We explored the genetic basis common to ticks, including heme and hemoglobin digestion, iron metabolism, and reactive oxygen species, and unveiled for the first time that genetic structure and pathogen composition in different tick species are mainly shaped by ecological and geographic factors. We further identified species-specific determinants associated with different host ranges, life cycles, and distributions. The findings of this study are an invaluable resource for research and control of ticks and tick-borne diseases.

Keywords

genetic diversity genome hematophagy metagenome tick tick-borne pathogen vector capacity

Grants

  1. BB/P024270/1/Biotechnology and Biological Sciences Research Council

MeSH Term

Animals
Cell Line
Disease Vectors
Genetic Variation
Host Specificity
Tick-Borne Diseases
Ticks
Comparative Study Journal Article Research Support, Non-U.S. Gov't

Links to CNCB-NGDC Resources

GWH: GWHAMMI00000000 (Haemaphysalis longicornis)
GWH: GWHAMML00000000 (Dermacentor silvarum)
GWH: GWHAMMK00000000 (Hyalomma asiaticum)
GWH: GWHAMMM00000000 (Rhipicephalus sanguineus)
GWH: GWHAMMN00000000 (Rhipicephalus microplus)
GWH: GWHAMMH00000000.1 ()
BioProject: PRJCA002242 (Population structure and genetic diversity of six tick specie)
GSA: CRA002715 (Population structure and genetic diversity of six tick species)
Article has an altmetric score of 55

Word Cloud

Created with Highcharts 10.0.0tickgeneticticksspeciespathogendiversitystructuredifferenttick-borneAmongarthropodvectorstransmitdiversehumananimalpathogensleadingincreasingnumbernewchallengesworldwidesequencedassembledhigh-qualitygenomessixixodidresequenced678specimensunderstandthreekeyaspectsticks:populationdistributionexploredbasiscommonincludinghemehemoglobindigestionironmetabolismreactiveoxygenunveiledfirsttimecompositionmainlyshapedecologicalgeographicfactorsidentifiedspecies-specificdeterminantsassociatedhostrangeslifecyclesdistributionsfindingsstudyinvaluableresourceresearchcontroldiseasesLarge-ScaleComparativeAnalysesTickGenomesElucidateGeneticDiversityVectorCapacitiesgenomehematophagymetagenomevectorcapacity

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