RNA virome analysis of Haemaphysalis longicornis ticks collected in Hyogo, Japan
Tick-borne viruses are primarily transmitted to vertebrates by infected ticks during blood feeding and cause various diseases in humans and animals. Haemaphysalis longicornis is one of the main tick species responsible for human tick bites and is thought to be the primary vector of severe fever with...
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| Published in | Japanese Journal of Infectious Diseases p. JJID.2025.027 |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Japan
National Institute of Infectious Diseases
30.06.2025
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| Abstract | Tick-borne viruses are primarily transmitted to vertebrates by infected ticks during blood feeding and cause various diseases in humans and animals. Haemaphysalis longicornis is one of the main tick species responsible for human tick bites and is thought to be the primary vector of severe fever with thrombocytopenia syndrome, an important tick-borne viral disease in Japan. Although H. longicornis ticks pose a potential risk to humans in Japan, studies on tick-borne viral prevalence of this tick species in Japan are limited. In this study, we conducted RNA virome analysis of H. longicornis ticks collected in Toyooka City, Hyogo Prefecture, Japan. Two known viruses, Dabieshan tick virus and Hubei sobemo-like virus 15, and putative novel quaranjavirus-like sequences were detected. Additionally, assessments of endogenous viral elements (EVEs) related to the virus and virus-like sequences suggested putative novel quaranjavirus-like sequences existed in both RNA and DNA forms. However, we could not determine whether this quaranjavirus-like sequence was of viral origin and could not conclude whether the DNA forms of the quaranjavirus-like sequence existed as EVEs in ticks. This study provides new insights into the prevalence of tick-associated viruses in ixodid ticks and serves as a reference for future approaches to prevent tick-borne diseases. |
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| AbstractList | Tick-borne viruses are primarily transmitted to vertebrates by infected ticks during blood feeding and cause various diseases in humans and animals. Haemaphysalis longicornis is one of the main tick species responsible for human tick bites and is thought to be the primary vector of severe fever with thrombocytopenia syndrome, an important tick-borne viral disease in Japan. Although H. longicornis ticks pose a potential risk to humans in Japan, studies on tick-borne viral prevalence of this tick species in Japan are limited. In this study, we conducted RNA virome analysis of H. longicornis ticks collected in Toyooka City, Hyogo Prefecture, Japan. Two known viruses, Dabieshan tick virus and Hubei sobemo-like virus 15, and putative novel quaranjavirus-like sequences were detected. Additionally, assessments of endogenous viral elements (EVEs) related to the virus and virus-like sequences suggested putative novel quaranjavirus-like sequences existed in both RNA and DNA forms. However, we could not determine whether this quaranjavirus-like sequence was of viral origin and could not conclude whether the DNA forms of the quaranjavirus-like sequence existed as EVEs in ticks. This study provides new insights into the prevalence of tick-associated viruses in ixodid ticks and serves as a reference for future approaches to prevent tick-borne diseases. Tick-borne viruses are primarily transmitted to vertebrates by infected ticks during blood feeding and cause various diseases in humans and animals. Haemaphysalis longicornis is one of the main tick species responsible for human tick bites and is thought to be the primary vector of severe fever with thrombocytopenia syndrome, an important tick-borne viral disease in Japan. Although H. longicornis ticks pose a potential risk to humans in Japan, studies on tick-borne viral prevalence of this tick species in Japan are limited. In this study, we conducted RNA virome analysis of H. longicornis ticks collected in Toyooka City, Hyogo Prefecture, Japan. Two known viruses, Dabieshan tick virus and Hubei sobemo-like virus 15, and putative novel quaranjavirus-like sequences were detected. Additionally, assessments of endogenous viral elements (EVEs) related to the virus and virus-like sequences suggested putative novel quaranjavirus-like sequences existed in both RNA and DNA forms. However, we could not determine whether this quaranjavirus-like sequence was of viral origin and could not conclude whether the DNA forms of the quaranjavirus-like sequence existed as EVEs in ticks. This study provides new insights into the prevalence of tick-associated viruses in ixodid ticks and serves as a reference for future approaches to prevent tick-borne diseases.Tick-borne viruses are primarily transmitted to vertebrates by infected ticks during blood feeding and cause various diseases in humans and animals. Haemaphysalis longicornis is one of the main tick species responsible for human tick bites and is thought to be the primary vector of severe fever with thrombocytopenia syndrome, an important tick-borne viral disease in Japan. Although H. longicornis ticks pose a potential risk to humans in Japan, studies on tick-borne viral prevalence of this tick species in Japan are limited. In this study, we conducted RNA virome analysis of H. longicornis ticks collected in Toyooka City, Hyogo Prefecture, Japan. Two known viruses, Dabieshan tick virus and Hubei sobemo-like virus 15, and putative novel quaranjavirus-like sequences were detected. Additionally, assessments of endogenous viral elements (EVEs) related to the virus and virus-like sequences suggested putative novel quaranjavirus-like sequences existed in both RNA and DNA forms. However, we could not determine whether this quaranjavirus-like sequence was of viral origin and could not conclude whether the DNA forms of the quaranjavirus-like sequence existed as EVEs in ticks. This study provides new insights into the prevalence of tick-associated viruses in ixodid ticks and serves as a reference for future approaches to prevent tick-borne diseases. |
| ArticleNumber | JJID.2025.027 |
| Author | Watanabe, Mamoru Sasaki, Toshinori Matsumura, Ryo Aboshi, Alisa Rose Itoyama, Kyo Kobayashi, Daisuke Isawa, Haruhiko Sawabe, Kyoko Inumaru, Mizue |
| Author_xml | – sequence: 1 fullname: Aboshi, Alisa Rose organization: School of Agriculture, Meiji University, Japan – sequence: 2 fullname: Matsumura, Ryo organization: School of Agriculture, Meiji University, Japan – sequence: 3 fullname: Inumaru, Mizue organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan – sequence: 4 fullname: Sawabe, Kyoko organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan – sequence: 5 fullname: Watanabe, Mamoru organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan – sequence: 6 fullname: Sasaki, Toshinori organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan – sequence: 7 fullname: Kobayashi, Daisuke organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan – sequence: 8 fullname: Itoyama, Kyo organization: School of Agriculture, Meiji University, Japan – sequence: 9 fullname: Isawa, Haruhiko organization: Department of Medical Entomology, National Institute of Infectious Diseases, Japan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40582886$$D View this record in MEDLINE/PubMed |
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| References | 20. Katoh K, Misawa K, Kuma KI, et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002: 30, 3059-3066. 26. Maketa H, Kobayashi I, Okabayashi T. Detection and phylogenetic analysis of Dabieshan tick virus and Okutama tick virus in ticks collected from Cape Toi, Japan. Ticks Tick Borne Dis. 2023: 14. 5. Kim KH, Yi J, Kim G, et al. Severe fever with thrombocytopenia syndrome, South Korea, 2012. Emerg Infect Dis. 2013: 19, 11. 17. Russo AG, Kelly AG, Tuipulotu DE, et al. Novel insights into endogenous RNA viral elements in Ixodes scapularis and other arbovirus vector genomes. Virus Evol. 2019: 5, vez010. 8. Kobayashi D, Murota K, Itokawa K, et al. RNA virome analysis of questing ticks from Hokuriku District, Japan, and the evolutionary dynamics of tick-borne phleboviruses. Ticks Tick Borne Dis. 2020: 11, 101364. 10. Luo LM, Zhao L, Wen HL, et al. Haemaphysalis longicornis ticks as reservoir and vector of severe fever with thrombocytopenia syndrome virus in China. Emerg Infect Dis. 2015: 21, 10. 7. Kosoy OI, Lambert AJ, Hawkinson DJ, et al. Novel thogotovirus associated with febrile illness and death, United States, 2014. Emerg Infect Dis. 2015: 21, 5. 11. Natsuaki M, Tick bites in Japan. J Dermatol. 2021: 48, 423-430. 6. Kobayashi Y, Kato H, Yamagishi T, et al. Severe fever with thrombocytopenia syndrome, Japan, 2013–2017. Emerg Infect Dis. 2020: 26, 4. 22. Felsenstein J. Phylogenies and the comparative method. Am Nat. 1985: 125, 1-15. 24. Shi M, Lin XD, Tian JH, et al. Redefining the invertebrate RNA virosphere. Nature. 2016: 540, 539-543. 39. Presti RM, Zhao G, Beatty WL, et al. Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol. 2009: 83, 11599-11606. 3. Yu XJ, Liang MF, Zhang SY, et al. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med. 2011: 364, 16. 25. Xu L, Guo M, Hu B, et al. Tick virome diversity in Hubei Province, China, and the influence of host ecology. Virus Evol. 2021: 7, veab089. 33. Yun Y, Heo ST, Kim G, et al. Phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in South Korea and migratory bird routes between China, South Korea, and Japan. Am J Trop Med Hyg. 2015: 93, 468-474. 12. Shao L, Pang Z, Fu H, et al. Identification of recently identified tick-borne viruses (Dabieshan tick virus and SFTSV) by metagenomic analysis in ticks from Shandong province, China. J Infect. 2020: 81, 973-978. 1. Madison-Antenucci S, Kramer L.D, Gebhardt L.L, et al. Emerging tick-borne diseases. Clin Microbiol Rev. 2020: 33, 2. 21. Kumar S, Stecher G, Li M, et al. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mil Biol Evol. 2018: 35, 1547-1549. 38. Dolja VV, Koonin EV. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res. 2018: 244, 36-52. 18. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019: 20, 1160-1166. 34. Ma C, Zhang R, Zhou H, et al. Prevalence and genetic diversity of Dabieshan tick virus in Shandong Province, China. J Infect. 2022: 85, 90-122. 32. Ministry of the Environment, Government of Japan. Survey of migratory bird flights. Available at <https://www.env.go.jp/nature/dobutsu/bird_flu/migratory/ap_wr_transit/index.html>. Accessed June 6, 2024. 27. Kobayashi D, Kuwata R, Kimura T, et al. Detection of quaranjavirus-like sequences from Haemaphysalis hystricis ticks collected in Japan. Jpn J Infect Dis. 2022: 75, 195-198. 13. Yang Z, Zhang J, Yang S, et al. Virome analysis of ticks in a forest region of Liaoning, China: characterization of a novel hepe-like virus sequence. Virol J. 2021: 18, 163. 14. Itokawa K, Sekizuka T, Maekawa Y, et al. High-throughput genotyping of a full voltage-gated sodium channel gene via genomic DNA using target capture sequencing and analytical pipeline MoNaS to discover novel insecticide resistance mutations. PLoS Negl Trop Dis. 2019: 13, 11. 16. Barnes M, Price DC. Endogenous viral elements in Ixodid tick genomes. Viruses. 2023: 15, 2201. 37. Tamm T, Truve E. Sobemoviruses. J Virol. 2000: 74, 6231-6241. 28. Sameroff S, Tokarz R, Jain K, et al. Novel quaranjavirus and other viral sequences identified from ticks parasitizing hunted wildlife in Trinidad and Tobago. Ticks Tick Borne Dis. 2021: 12. 29. Guo L, Ma J, Lin J, et al. Virome of Rhipicephalus ticks by metagenomic analysis in Guangdong, southern China. Front. Microbiol. 2022: 13, 966735. 30. Bratuleanu BE, Temmam S, Munier S, et al. Detection of Phenuiviridae, Chuviridae members, and a novel quaranjavirus in hard ticks from Danube Delta. Front Vet Sci. 2022: 9, 863814. 2. McMullan LK, Folk SM, Kelly AJ, et al. A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med. 2012: 367, 834-841. 4. Takahashi T, Maeda K, Suzuki, T, et al. The first identification and retrospective study of severe fever with thrombocytopenia syndrome in Japan. J. Infect Dis. 2013: 209, 816-827. 31. Yong DL, Liu Y, Low BW, et al. Migratory songbirds in the East Asian-Australasian Flyway: a review from a conservation perspective. Bird Conserv Int. 2015: 25, 1-37. 15. Kobayashi D, Komatsu N, Faizah AN, et al. A novel nyavirus lacking matrix and glycoprotein genes from Argas japonicus ticks. Virus Res. 2021: 292, 198254. 23. Li CX, Shi M, Tian JH, et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife. 2015: 4, e05378. 9. Matsumura R, Kobayashi D, Itoyama K, et al. Detection of novel coltivirus-related sequences in Haemaphysalis megaspinosa ticks collected from Kanagawa Prefecture, Japan. J Vet Med Sci. 2024: 86, 866-871. 19. Katoh K, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005: 33, 511-518. 40. Salvati MV, Salaris C, Monteil V, et al. Virus-derived DNA forms mediate the persistent infection of tick cells by Hazara virus and Crimean-Congo hemorrhagic fever virus. J Virol. 2021: 95, e01638-21. 35. Qin T, Shi M, Zhang M, et al. Diversity of RNA viruses of three dominant tick species in North China. Front Vet Sci. 2023: 13, 1057977. 36. Ye RZ, Li YY, Xu DL, et al. Virome diversity shaped by genetic evolution and ecological landscape of Haemaphysalis longicornis. Microbiome. 2024: 12, 35. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 34 13 35 14 36 15 37 16 38 17 39 18 19 1 2 3 4 5 6 7 8 9 40 20 21 |
| References_xml | – reference: 19. Katoh K, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005: 33, 511-518. – reference: 24. Shi M, Lin XD, Tian JH, et al. Redefining the invertebrate RNA virosphere. Nature. 2016: 540, 539-543. – reference: 38. Dolja VV, Koonin EV. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res. 2018: 244, 36-52. – reference: 11. Natsuaki M, Tick bites in Japan. J Dermatol. 2021: 48, 423-430. – reference: 37. Tamm T, Truve E. Sobemoviruses. J Virol. 2000: 74, 6231-6241. – reference: 15. Kobayashi D, Komatsu N, Faizah AN, et al. A novel nyavirus lacking matrix and glycoprotein genes from Argas japonicus ticks. Virus Res. 2021: 292, 198254. – reference: 39. Presti RM, Zhao G, Beatty WL, et al. Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol. 2009: 83, 11599-11606. – reference: 10. Luo LM, Zhao L, Wen HL, et al. Haemaphysalis longicornis ticks as reservoir and vector of severe fever with thrombocytopenia syndrome virus in China. Emerg Infect Dis. 2015: 21, 10. – reference: 40. Salvati MV, Salaris C, Monteil V, et al. Virus-derived DNA forms mediate the persistent infection of tick cells by Hazara virus and Crimean-Congo hemorrhagic fever virus. J Virol. 2021: 95, e01638-21. – reference: 31. Yong DL, Liu Y, Low BW, et al. Migratory songbirds in the East Asian-Australasian Flyway: a review from a conservation perspective. Bird Conserv Int. 2015: 25, 1-37. – reference: 36. Ye RZ, Li YY, Xu DL, et al. Virome diversity shaped by genetic evolution and ecological landscape of Haemaphysalis longicornis. Microbiome. 2024: 12, 35. – reference: 17. Russo AG, Kelly AG, Tuipulotu DE, et al. Novel insights into endogenous RNA viral elements in Ixodes scapularis and other arbovirus vector genomes. Virus Evol. 2019: 5, vez010. – reference: 2. McMullan LK, Folk SM, Kelly AJ, et al. A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med. 2012: 367, 834-841. – reference: 5. Kim KH, Yi J, Kim G, et al. Severe fever with thrombocytopenia syndrome, South Korea, 2012. Emerg Infect Dis. 2013: 19, 11. – reference: 32. Ministry of the Environment, Government of Japan. Survey of migratory bird flights. Available at <https://www.env.go.jp/nature/dobutsu/bird_flu/migratory/ap_wr_transit/index.html>. Accessed June 6, 2024. – reference: 12. Shao L, Pang Z, Fu H, et al. Identification of recently identified tick-borne viruses (Dabieshan tick virus and SFTSV) by metagenomic analysis in ticks from Shandong province, China. J Infect. 2020: 81, 973-978. – reference: 1. Madison-Antenucci S, Kramer L.D, Gebhardt L.L, et al. Emerging tick-borne diseases. Clin Microbiol Rev. 2020: 33, 2. – reference: 34. Ma C, Zhang R, Zhou H, et al. Prevalence and genetic diversity of Dabieshan tick virus in Shandong Province, China. J Infect. 2022: 85, 90-122. – reference: 3. Yu XJ, Liang MF, Zhang SY, et al. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med. 2011: 364, 16. – reference: 6. Kobayashi Y, Kato H, Yamagishi T, et al. Severe fever with thrombocytopenia syndrome, Japan, 2013–2017. Emerg Infect Dis. 2020: 26, 4. – reference: 22. Felsenstein J. Phylogenies and the comparative method. Am Nat. 1985: 125, 1-15. – reference: 7. Kosoy OI, Lambert AJ, Hawkinson DJ, et al. Novel thogotovirus associated with febrile illness and death, United States, 2014. Emerg Infect Dis. 2015: 21, 5. – reference: 33. Yun Y, Heo ST, Kim G, et al. Phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in South Korea and migratory bird routes between China, South Korea, and Japan. Am J Trop Med Hyg. 2015: 93, 468-474. – reference: 29. Guo L, Ma J, Lin J, et al. Virome of Rhipicephalus ticks by metagenomic analysis in Guangdong, southern China. Front. Microbiol. 2022: 13, 966735. – reference: 35. Qin T, Shi M, Zhang M, et al. Diversity of RNA viruses of three dominant tick species in North China. Front Vet Sci. 2023: 13, 1057977. – reference: 20. Katoh K, Misawa K, Kuma KI, et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002: 30, 3059-3066. – reference: 8. Kobayashi D, Murota K, Itokawa K, et al. RNA virome analysis of questing ticks from Hokuriku District, Japan, and the evolutionary dynamics of tick-borne phleboviruses. Ticks Tick Borne Dis. 2020: 11, 101364. – reference: 9. Matsumura R, Kobayashi D, Itoyama K, et al. Detection of novel coltivirus-related sequences in Haemaphysalis megaspinosa ticks collected from Kanagawa Prefecture, Japan. J Vet Med Sci. 2024: 86, 866-871. – reference: 25. Xu L, Guo M, Hu B, et al. Tick virome diversity in Hubei Province, China, and the influence of host ecology. Virus Evol. 2021: 7, veab089. – reference: 13. Yang Z, Zhang J, Yang S, et al. Virome analysis of ticks in a forest region of Liaoning, China: characterization of a novel hepe-like virus sequence. Virol J. 2021: 18, 163. – reference: 4. Takahashi T, Maeda K, Suzuki, T, et al. The first identification and retrospective study of severe fever with thrombocytopenia syndrome in Japan. J. Infect Dis. 2013: 209, 816-827. – reference: 16. Barnes M, Price DC. Endogenous viral elements in Ixodid tick genomes. Viruses. 2023: 15, 2201. – reference: 21. Kumar S, Stecher G, Li M, et al. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mil Biol Evol. 2018: 35, 1547-1549. – reference: 14. Itokawa K, Sekizuka T, Maekawa Y, et al. High-throughput genotyping of a full voltage-gated sodium channel gene via genomic DNA using target capture sequencing and analytical pipeline MoNaS to discover novel insecticide resistance mutations. PLoS Negl Trop Dis. 2019: 13, 11. – reference: 27. Kobayashi D, Kuwata R, Kimura T, et al. 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| Title | RNA virome analysis of Haemaphysalis longicornis ticks collected in Hyogo, Japan |
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