TY - JOUR
T1 - The evolution of hard tick-borne relapsing fever borreliae is correlated with vector species rather than geographical distance
AU - Nakao, Ranna
AU - Kasama, Kentaro
AU - Boldbaatar, Bazartseren
AU - Ogura, Yoshitoshi
AU - Kawabata, Hiroki
AU - Toyoda, Atsushi
AU - Hayashi, Tetsuya
AU - Takano, Ai
AU - Maeda, Ken
N1 - Funding Information:
We thank Dr. Minoru Nakao (Asahikawa Medical University) for providing B. miyamotoi strains, Mr. Nyamdorj Erdenebat (Center for Zoonotic Diseases) for collecting ticks in Mongolia. We thank Prof. Masahiro Fujishima (Yamaguchi University) for the use of laboratory equipment and Prof. DeMar Taylor (Tsukuba University) for assistance with editing this manuscript. We would like to thank Ms. Kiwa Furuno, Nana Ito, and Yoshiko Inagaki for their technical assistance. We also acknowledge the technical expertise of the DNA Core facility at the Center for Gene Research, Yamaguchi University, which was supported by a grant-in-aid from the Ministry of Education, Science, Sports and Culture of Japan.
Funding Information:
A.Ta., T.H. and H.K. received funding from the Research Program on Emerging and Re-emerging Infectious Diseases (Grant ID JP20fk0108068 and 21fk0108614) from the Japan Agency for Medical Research and Development (AMED).
Funding Information:
We thank Dr. Minoru Nakao (Asahikawa Medical University) for providing B. miyamotoi strains, Mr. Nyamdorj Erdenebat (Center for Zoonotic Diseases) for collecting ticks in Mongolia. We thank Prof. Masahiro Fujishima (Yamaguchi University) for the use of laboratory equipment and Prof. DeMar Taylor (Tsukuba University) for assistance with editing this manuscript. We would like to thank Ms. Kiwa Furuno, Nana Ito, and Yoshiko Inagaki for their technical assistance. We also acknowledge the technical expertise of the DNA Core facility at the Center for Gene Research, Yamaguchi University, which was supported by a grant-in-aid from the Ministry of Education, Science, Sports and Culture of Japan.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - 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.
AB - 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.
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U2 - 10.1186/s12862-021-01838-1
DO - 10.1186/s12862-021-01838-1
M3 - Article
C2 - 34058972
AN - SCOPUS:85107322296
VL - 21
JO - BMC Ecology and Evolution
JF - BMC Ecology and Evolution
SN - 1472-6785
IS - 1
M1 - 105
ER -