Identification and epidemiological study of an uncultured flavivirus from ticks using viral metagenomics and pseudoinfectious viral particles

Author:

Kobayashi Daisuke12,Inoue Yusuke34,Suzuki Ryosuke5,Matsuda Mami5,Shimoda Hiroshi4,Faizah Astri Nur1ORCID,Kaku Yoshihiro3,Ishijima Keita3,Kuroda Yudai34,Tatemoto Kango34,Virhuez-Mendoza Milagros34,Harada Michiko34,Nishino Ayano34,Inumaru Mizue1ORCID,Yonemitsu Kenzo24,Kuwata Ryusei46ORCID,Takano Ai4ORCID,Watanabe Mamoru1,Higa Yukiko1,Sawabe Kyoko12,Maeda Ken34ORCID,Isawa Haruhiko1

Affiliation:

1. Department of Medical Entomology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan

2. Management Department of Biosafety, Laboratory Animal, and Pathogen Bank, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan

3. Department of Veterinary Science, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan

4. Joint Graduate School of Veterinary Medicine, Yamaguchi University, Yamaguchi City, Yamaguchi 753-8515, Japan

5. Department of Virology II, National Institute of Infectious Diseases, Musashimurayama City, Tokyo 208-0011, Japan

6. Faculty of Veterinary Medicine, Okayama University of Science, Imabari City, Ehime 794-8555, Japan

Abstract

During their blood-feeding process, ticks are known to transmit various viruses to vertebrates, including humans. Recent viral metagenomic analyses using next-generation sequencing (NGS) have revealed that blood-feeding arthropods like ticks harbor a large diversity of viruses. However, many of these viruses have not been isolated or cultured, and their basic characteristics remain unknown. This study aimed to present the identification of a difficult-to-culture virus in ticks using NGS and to understand its epidemic dynamics using molecular biology techniques. During routine tick-borne virus surveillance in Japan, an unknown flaviviral sequence was detected via virome analysis of host-questing ticks. Similar viral sequences have been detected in the sera of sika deer and wild boars in Japan, and this virus was tentatively named the Saruyama virus (SAYAV). Because SAYAV did not propagate in any cultured cells tested, single-round infectious virus particles (SRIP) were generated based on its structural protein gene sequence utilizing a yellow fever virus-based replicon system to understand its nationwide endemic status. Seroepidemiological studies using SRIP as antigens have demonstrated the presence of neutralizing antibodies against SAYAV in sika deer and wild boar captured at several locations in Japan, suggesting that SAYAV is endemic throughout Japan. Phylogenetic analyses have revealed that SAYAV forms a sister clade with the Orthoflavivirus genus, which includes important mosquito- and tick-borne pathogenic viruses. This shows that SAYAV evolved into a lineage independent of the known orthoflaviviruses. This study demonstrates a unique approach for understanding the epidemiology of uncultured viruses by combining viral metagenomics and pseudoinfectious viral particles.

Funder

Japan Agency for Medical Research and Development

MEXT | Japan Science and Technology Agency

Regulatory Science Research from Ministry of Health, Labor and Welfare

MEXT | Japan Society for the Promotion of Science

Publisher

Proceedings of the National Academy of Sciences

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