Comparative genomics reveals unique features of two Babesia motasi subspecies: Babesia motasi lintanensis and Babesia motasi hebeiensis

Jinming Wang; Kai Chen; Qiaoyun Ren; Shangdi Zhang; Jifei Yang; Yanbo Wang; Yueli Nian; Xiaoyun Li; Guangyuan Liu; Jianxun Luo; Hong Yin; Guiquan Guan

doi:10.1016/j.ijpara.2023.02.005

Comparative genomics reveals unique features of two Babesia motasi subspecies: Babesia motasi lintanensis and Babesia motasi hebeiensis

Int J Parasitol. 2023 May;53(5-6):265-283. doi: 10.1016/j.ijpara.2023.02.005. Epub 2023 Mar 31.

Authors

Jinming Wang¹, Kai Chen², Qiaoyun Ren³, Shangdi Zhang⁴, Jifei Yang⁵, Yanbo Wang⁶, Yueli Nian⁷, Xiaoyun Li⁸, Guangyuan Liu⁹, Jianxun Luo¹⁰, Hong Yin¹¹, Guiquan Guan¹²

Affiliations

¹ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: wjm0403@caas.cn.
² Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China. Electronic address: chenkai@ihb.ac.cn.
³ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: renqiaoyun@caas.cn.
⁴ Department of Clinical Laboratory, The Second Hospital of Lanzhou University, Lanzhou, China. Electronic address: zhangsd1985@126.com.
⁵ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: yangjifei@caas.cn.
⁶ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China; Department of Clinical Laboratory, The Second Hospital of Lanzhou University, Lanzhou, China. Electronic address: wangyb2020@lzu.edu.cn.
⁷ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China; Department of Clinical Laboratory, The Second Hospital of Lanzhou University, Lanzhou, China. Electronic address: nianyl21@lzu.edu.cn.
⁸ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: 2261828147@qq.com.
⁹ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: liuguangyuan@caas.cn.
¹⁰ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: luojianxun@caas.cn.
¹¹ State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China; Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou University, Yangzhou 225009, China. Electronic address: yinhong@caas.cn.
¹² State Key Laboratory for Animal Disease Control and Prevention, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Lanzhou, Gansu 730046, China. Electronic address: guanguiquan@caas.cn.

PMID: 37004737
DOI: 10.1016/j.ijpara.2023.02.005

Abstract

Parasites of the Babesia genus are prevalent worldwide and infect a wide diversity of domestic animals and humans. Herein, using Oxford Nanopore Technology and Illumina sequencing technologies, we sequenced two Babesia subspecies, Babesia motasi lintanensis and Babesia motasi hebeiensis. We identified 3,815 one-to-one ortholog genes that are specific to ovine Babesia spp. Phylogenetic analysis reveals that the two B. motasi subspecies form a distinct clade from other piroplasmas. Consistent with their phylogenetic position, comparative genomic analysis reveals that these two ovine Babesia spp. share higher colinearity with Babesia bovis than with Babesia microti. Concerning the speciation date, B. m. lintanensis split from B. m. hebeiensis approximately 17 million years ago. Genes correlated to transcription, translation, protein modification and degradation, as well as differential/specialized gene family expansions in these two subspecies may favor adaptation to vertebrate and tick hosts. The close relationship between B. m. lintanensis and B. m. hebeiensis is underlined by a high degree of genomic synteny. Compositions of most invasion, virulence, development, and gene transcript regulation-related multigene families, including spherical body protein, variant erythrocyte surface antigen, glycosylphosphatidylinositol anchored proteins, and transcription factor Apetala 2 genes, is largely conserved, but in contrast to this conserved situation, we observe major differences in species-specific genes that may be involved in multiple functions in parasite biology. For the first time in Babesia spp., we find abundant fragments of long terminal repeat-retrotransposons in these two species. We provide fundamental information to characterize the genomes of B. m. lintanensis and B. m. hebeiensis, providing insights into the evolution of B. motasi group parasites.

Keywords: Adaptive evolution; Babesia motasi; Glycosylphosphatidylinositol anchored protein; Long terminal repeat (LTR)-retrotransposon; Multigene families; Phylogenetic analysis; Retrotransposon.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Babesia bovis*
Babesia microti*
Babesia* / genetics
Babesiosis* / parasitology
Genomics
Humans
Phylogeny
Sheep