Ranna Nakao1, Kentaro Kasama2, Bazartseren Boldbaatar3, Yoshitoshi Ogura4, Hiroki Kawabata5, Atsushi Toyoda6, Tetsuya Hayashi2, Ai Takano7,8, Ken Maeda9,10. 1. Department of Veterinary Medicine, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi City, Yamaguchi, 753-8515, Japan. 2. Department of Bacteriology, Faculty of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka City, Fukuoka, 812-8582, Japan. 3. Laboratory of Virology, Institute of Veterinary Medicine, Mongolian University of Life Sciences, Zaisan, 17024, Ulaanbaatar, Mongolia. 4. Division of Microbiology, Department of Infectious Medicine, Kurume University School of Medicine, 67 Asahi-machi, Kurume City, Fukuoka, 830-0011, Japan. 5. Department of Bacteriology-I, National Institute of Infectious Disease, 1-23-1 Toyama, Shinjyuku-ku, Tokyo, 162-8640, Japan. 6. Department of Genomics and Evolutionary Biology, National Institute of Genetics, 1111 Yata, Mishima City, Shizuoka, 411-8540, Japan. 7. Department of Veterinary Medicine, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi City, Yamaguchi, 753-8515, Japan. a-takano@yamaguchi-u.ac.jp. 8. Joint Graduate School of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan. a-takano@yamaguchi-u.ac.jp. 9. Joint Graduate School of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan. 10. Department of Veterinary Science, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjyuku-ku, Tokyo, 162-8640, Japan.
Abstract
BACKGROUND: Relapsing fever (RF) borreliae are arthropod-borne spirochetes and some of them cause human diseases, which are characterized by relapsing or recurring episodes of fever. Recently, it has been classified into two groups: soft tick-borne RF (STRF) borreliae and hard tick-borne RF (HTRF) borreliae. STRF borreliae include classical RF agents and HTRF borreliae, the latter of which include B. miyamotoi, a human pathogen recently identified in Eurasia and North America. RESULTS: In this study, we determined the genome sequences of 16 HTRF borreliae strains: 15 B. miyamotoi strains (9 from Hokkaido Island, Japan, 3 from Honshu Island, Japan, and 3 from Mongolia) and a Borrelia sp. tHM16w. Chromosomal gene synteny was highly conserved among the HTRF strains sequenced in this study, even though they were isolated from different geographic regions and different tick species. Phylogenetic analysis based on core gene sequences revealed that HTRF and STRF borreliae are clearly distinguishable, with each forming a monophyletic group in the RF borreliae lineage. Moreover, the evolutionary relationships of RF borreliae are consistent with the biological and ecological features of each RF borreliae sublineage and can explain the unique characteristics of Borrelia anserina. In addition, the pairwise genetic distances between HTRF borreliae strains were well correlated with those of vector species rather than with the geographical distances between strain isolation sites. This result suggests that the genetic diversification of HTRF borreliae is attributed to the speciation of vector ticks and that this relationship might be required for efficient transmission of HTRF borreliae within vector ticks. CONCLUSIONS: The results of the present study, together with those from previous investigations, support the hypothesis that the common ancestor of borreliae was transmitted by hard-bodied ticks and that only STRF borreliae switched to using soft-bodied ticks as a vector, which was followed by the emergence of Borrelia recurrentis, lice-borne RF borreliae. Our study clarifies the phylogenetic relationships between RF borreliae, and the data obtained will contribute to a better understanding of the evolutionary history of RF borreliae.
BACKGROUND:Relapsingfever (RF) borreliae are arthropod-borne spirochetes and some of them cause human diseases, which are characterized by relapsing or recurring episodes of fever. Recently, it has been classified into two groups: soft tick-borne RF (STRF) borreliae and hard tick-borne RF (HTRF) borreliae. STRF borreliae include classical RF agents and HTRF borreliae, the latter of which include B. miyamotoi, a human pathogen recently identified in Eurasia and North America. RESULTS: In this study, we determined the genome sequences of 16 HTRF borreliae strains: 15 B. miyamotoi strains (9 from Hokkaido Island, Japan, 3 from Honshu Island, Japan, and 3 from Mongolia) and a Borrelia sp. tHM16w. Chromosomal gene synteny was highly conserved among the HTRF strains sequenced in this study, even though they were isolated from different geographic regions and different tick species. Phylogenetic analysis based on core gene sequences revealed that HTRF and STRF borreliae are clearly distinguishable, with each forming a monophyletic group in the RF borreliae lineage. Moreover, the evolutionary relationships of RF borreliae are consistent with the biological and ecological features of each RF borreliae sublineage and can explain the unique characteristics of Borrelia anserina. In addition, the pairwise genetic distances between HTRF borreliae strains were well correlated with those of vector species rather than with the geographical distances between strain isolation sites. This result suggests that the genetic diversification of HTRF borreliae is attributed to the speciation of vector ticks and that this relationship might be required for efficient transmission of HTRF borreliae within vector ticks. CONCLUSIONS: The results of the present study, together with those from previous investigations, support the hypothesis that the common ancestor of borreliae was transmitted by hard-bodied ticks and that only STRF borreliae switched to using soft-bodied ticks as a vector, which was followed by the emergence of Borrelia recurrentis, lice-borne RF borreliae. Our study clarifies the phylogenetic relationships between RF borreliae, and the data obtained will contribute to a better understanding of the evolutionary history of RF borreliae.
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