Mitochondrial Genome Analysis of Babesia ovis (Apicomplexa: Babesiidae) Endemic in Sheep in Türkiye
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Parasites and Isolation of Genomic DNA
2.2. Amplification of B. ovis Mitochondrial Genome and Sequence Analyzing
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Attardi, G.; Schatz, G. Biogenesis of mitochondria. Annu. Rev. Cell Biol. 1988, 4, 289–331. [Google Scholar] [CrossRef] [PubMed]
- Hikosaka, K.; Watanabe, Y.; Kobayashi, F.; Waki, S.; Kita, K.; Tanabe, K. Highly conserved gene arrangement of the mitochondrial genomes of 23 Plasmodium species. Parasitol. Int. 2011, 60, 175–180. [Google Scholar] [CrossRef] [PubMed]
- Lang, B.F.; Gray, M.W.; Burger, G. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 1999, 33, 351–397. [Google Scholar] [CrossRef] [PubMed]
- Schreeg, M.E.; Marr, H.S.; Tarigo, J.L.; Cohn, L.A.; Bird, D.M.; Scholl, E.H.; Levy, M.G.; Wiegmann, B.M.; Birkenheuer, A.J. Mitochondrial genome sequences and structures aid in the resolution of piroplasmida phylogeny. PLoS ONE 2016, 11, e0165702. [Google Scholar] [CrossRef]
- Wang, X.; Wang, J.; Liu, J.; Liu, A.; He, X.; Xiang, Q.; Li, Y.; Yin, H.; Luo, J.; Guan, G. Insights into the phylogenetic relationships and drug targets of Babesia isolates infective to small ruminants from the mitochondrial genomes. Parasites Vectors 2020, 13, 378. [Google Scholar] [CrossRef]
- Boore, J.L. Animal mitochondrial genomes. Nucleic Acids Res. 1999, 27, 1767–1780. [Google Scholar] [CrossRef]
- Hikosaka, K.; Watanabe, Y.; Tsuji, N.; Kita, K.; Kishine, H.; Arisue, N.; Palacpac, N.M.Q.; Kawazu, S.; Sawai, H.; Horii, T. Divergence of the mitochondrial genome structure in the apicomplexan parasites, Babesia and Theileria. Mol. Biol. Evol. 2010, 27, 1107–1116. [Google Scholar] [CrossRef] [PubMed]
- Hikosaka, K.; Tsuji, N.; Watanabe, Y.; Kishine, H.; Horii, T.; Igarashi, I.; Kita, K.; Tanabe, K. Novel type of linear mitochondrial genomes with dual flip-flop inversion system in apicomplexan parasites, Babesia microti and Babesia rodhaini. BMC Genom. 2012, 13, 622. [Google Scholar] [CrossRef]
- Preiser, P.R.; Wilson, R.J.; Moore, P.W.; McCready, S.; Hajibagheri, M.A.; Blight, K.J.; Strath, M.; Williamson, D.H. Recombination associated with replication of malarial mitochondrial DNA. EMBO J. 1996, 15, 684–693. [Google Scholar] [CrossRef]
- Esseiva, A.C.; Naguleswaran, A.; Hemphill, A.; Schneider, A. Mitochondrial tRNA import in Toxoplasma gondii. J. Biol. Chem. 2004, 279, 42363–42368. [Google Scholar] [CrossRef]
- Rusconi, C.P.; Cech, T.R. Mitochondrial import of only one of three nuclear-encoded glutamine tRNAs in Tetrahymena thermophila. EMBO J. 1996, 15, 3286–3295. [Google Scholar] [CrossRef] [PubMed]
- Schnittger, L.; Ganzinelli, S.; Bhoora, R.; Omondi, D.; Nijhof, A.M.; Florin-Christensen, M. The piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: Species compilation, molecular phylogeny, and evolutionary insights. Parasitol. Res. 2022, 121, 1207–1245. [Google Scholar] [CrossRef] [PubMed]
- Uilenberg, G. Babesia—A Historical Overview. Vet. Parasitol. 2006, 138, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Ozubek, S.; Bastos, R.G.; Alzan, H.F.; Inci, A.; Aktas, M.; Suarez, C.E. Bovine babesiosis in Turkey: Impact, current gaps, and opportunities for intervention. Pathogens 2020, 9, 1041. [Google Scholar] [CrossRef]
- Firat, R.; Ulucesme, M.C.; Aktaş, M.; Ceylan, O.; Sevinc, F.; Bastos, R.G.; Suarez, C.E.; Ozubek, S. Role of Rhipicephalus bursa larvae in transstadial transmission and endemicity of Babesia ovis in chronically infected sheep. Front. Cell. Infect. Microbiol. 2024, 14, 1428719. [Google Scholar] [CrossRef]
- Sevinç, F.; Xuenan, X. Major Tick-borne parasitic diseases of animals: A frame of references in Turkey. Eurasian J. Vet. Sci. 2015, 31, 132–142. [Google Scholar] [CrossRef]
- Ceylan, O.; Xuan, X.; Sevinc, F. Primary tick-borne protozoan and rickettsial infections of animals in Turkey. Pathogens 2021, 10, 231. [Google Scholar] [CrossRef]
- Virji, A.Z.; Thekkiniath, J.; Ma, W.; Lawres, L.; Knight, J.; Swei, A.; Le Roch, K.; Mamoun, C.B. Insights into the evolution and drug susceptibility of Babesia duncani from the sequence of its mitochondrial and apicoplast genomes. Int. J. Parasitol. 2019, 49, 105–113. [Google Scholar] [CrossRef]
- He, L.; Zhang, Y.; Zhang, Q.-L.; Zhang, W.-J.; Feng, H.-H.; Khan, M.K.; Hu, M.; Zhou, Y.-Q.; Zhao, J.-L. Mitochondrial genome of Babesia orientalis, apicomplexan parasite of water buffalo (Bubalus babalis, Linnaeus, 1758) endemic in China. Parasites Vectors 2014, 7, 82. [Google Scholar] [CrossRef]
- Malandrin, L.; Jouglin, M.; Sun, Y.; Brisseau, N.; Chauvin, A. Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): Isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. Int. J. Parasitol. 2010, 40, 277–284. [Google Scholar] [CrossRef]
- Bonsergent, C.; de Carné, M.-C.; de La Cotte, N.; Moussel, F.; Perronne, V.; Malandrin, L. The New human Babesia sp. FR1 is a european member of the Babesia sp. MO1 clade. Pathogens 2021, 10, 1433. [Google Scholar] [CrossRef] [PubMed]
- Hikosaka, K.; Kita, K.; Tanabe, K. Diversity of mitochondrial genome structure in the phylum apicomplexa. Mol. Biochem. Parasitol. 2013, 188, 26–33. [Google Scholar] [CrossRef]
- Ozubek, S.; Ulucesme, M.C.; Aktas, M. Discovery of a novel species infecting goats: Morphological and molecular characterization of Babesia aktasi n. sp. Pathogens 2023, 12, 113. [Google Scholar] [CrossRef] [PubMed]
- Baneth, G.; Nachum-Biala, Y.; Birkenheuer, A.J.; Schreeg, M.E.; Prince, H.; Florin-Christensen, M.; Schnittger, L.; Aroch, I. A new piroplasmid species infecting dogs: Morphological and molecular characterization and pathogeny of Babesia negevi n. sp. Parasites Vectors 2020, 13, 130. [Google Scholar] [CrossRef]
- Sivakumar, T.; Tuvshintulga, B.; Otgonsuren, D.; Batmagnai, E.; Ahedor, B.; Kothalawala, H.; Vimalakumar, S.C.; Silva, S.S.P.; Yamagishi, J.; Yokoyama, N. Phylogenetic analyses of the mitochondrial, plastid, and nuclear genes of Babesia sp. mymensingh and its naming as Babesia naoakii n. sp. Parasites Vectors 2022, 15, 299. [Google Scholar] [CrossRef]
- Xiong, L.; Yang, G. Description and molecular characterisation of Babesia ailuropodae n. sp., a new piroplasmid species infecting giant pandas. Parasites Vectors 2024, 17, 315. [Google Scholar] [CrossRef]
- Ulucesme, M.C.; Ozubek, S.; Karoglu, A.; Turk, Z.I.; Olmus, I.; Irehan, B.; Aktas, M. Small ruminant piroplasmosis: High prevalence of Babesia aktasi n. sp. in goats in Türkiye. Pathogens 2023, 12, 514. [Google Scholar] [CrossRef] [PubMed]
- Ozubek, S.; Aktas, M. Molecular and parasitological survey of ovine piroplasmosis, including the first report of Theileria annulata (Apicomplexa: Theileridae) in sheep and goats from Turkey. J. Med. Entomol. 2017, 54, 212–220. [Google Scholar] [CrossRef]
- Ceylan, O.; Sevinc, F. Endemic instability of ovine babesiosis in Turkey: A country-wide sero-epidemiological study. Vet. Parasitol. 2020, 278, 109034. [Google Scholar] [CrossRef]
- Ozubek, S.; Aktas, M. Molecular evidence of a new Babesia sp. in goats. Vet. Parasitol. 2017, 233, 1–8. [Google Scholar] [CrossRef]
- Babraham Bioinformatics. FastQC A Quality Control Tool for High Throughput Sequence Data. Available online: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 30 June 2024).
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef] [PubMed]
- Le, S.Q.; Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 2008, 25, 1307–1320. [Google Scholar] [CrossRef]
- Jones, D.T.; Taylor, W.R.; Thornton, J.M. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 1992, 8, 275–282. [Google Scholar] [CrossRef]
- Tian, Z.; Gao, S.; Ren, Q.; Du, J.; Guan, G.; Liu, G.; Luo, J.; Yin, H. Mitochondrial genome of Theileria uilenbergi endemic in sheep and goats in China. Parasitol. Res. 2021, 120, 3429–3436. [Google Scholar] [CrossRef]
- Carrasco, M.P.; Gut, J.; Rodrigues, T.; Ribeiro, M.H.L.; Lopes, F.; Rosenthal, P.J.; Moreira, R.; dos Santos, D.J.V.A. Exploring the molecular basis of Qo bc1 complex inhibitors activity to find novel antimalarials Hits. Mol. Inform. 2013, 32, 659–670. [Google Scholar] [CrossRef] [PubMed]
- Birth, D.; Kao, W.-C.; Hunte, C. Structural analysis of atovaquone-inhibited cytochrome bc1 complex reveals the molecular basis of antimalarial drug action. Nat. Commun. 2014, 5, 4029. [Google Scholar] [CrossRef]
- Gjerde, B. Characterisation of full-length mitochondrial copies and partial nuclear copies (numts) of the cytochrome b and cytochrome c oxidase subunit i genes of Toxoplasma gondii, Neospora caninum, Hammondia heydorni and Hammondia triffittae (Apicomplexa: Sarcocystidae). Parasitol. Res. 2013, 112, 1493–1511. [Google Scholar] [CrossRef]
Primer Name | Primer Sequence (5′–3′) |
---|---|
MitoF1 | AACAAGTGATCATGTATAAAGTA |
Mitoseqfor1 | TGGGCTCATCATATGTACAC |
Mitoseqrev1 | GTGTACATATGATGAGCCCA |
MitoF2 | GCATGCAATACCGAACAGGGCCA |
MitoR1 | ACTCTATAGGTATTTGACGTAATT |
Mitoseq2for | TTATTTCAAATCTATATAGT |
Mitoseq3f | AGCCGATATAGAGTTTCA |
MitoR2 | TGTTCAACAGACGCTCCTCA |
MitoF3 | AACGACTTCTCTATTGTCTCCAC |
Mitoseqrev2 | TTCTTTGCCTTGGATGTCAAT |
MitoR3 | AATGAGTTATTGGGGAGC |
MitoR5 | TGTTAAAAAACTTTATATTTGTTGAAATTT |
Species | 5′ TIR | cox1 | cox3 | LSU1 | LSU3 | LSU6 | LSU2 | cytb (cob) | LSU5 | LSU4 | 3′ TIR | Total |
---|---|---|---|---|---|---|---|---|---|---|---|---|
B. ovis (PP973837) | 117 | 1434 | 639 | 303 | 111 | 38 | 36 | 1092 | 68 | 82 | 117 | 6015 |
B. bovis (AB499088) | 119 | 1434 | 639 | 302 | 111 | 38 | 35 | 1092 | 68 | 82 | 119 | 5970 |
B. bigemina (AB499085) | 65 | 1434 | 639 | 299 | 111 | 37 | 36 | 1092 | 70 | 82 | 65 | 5924 |
B. caballi (AB499086) | 62 | 1434 | 639 | 301 | 111 | 37 | 35 | 1092 | 68 | 82 | 62 | 5847 |
B. gibsoni (AB499087) | 74 | 1434 | 639 | 306 | 111 | 43 | 35 | 1092 | 70 | 82 | 74 | 5865 |
BspXJ (KX698108) | 25 | 1434 | 639 | 302 | 111 | 37 | 36 | 1092 | 69 | 82 | 25 | 6020 |
BmLT (KX698109) | 35 | 1434 | 639 | 297 | 111 | 37 | 36 | 1092 | 70 | 82 | 35 | 5790 |
BmNX (MN605891) | 101 | 1434 | 639 | 297 | 111 | 37 | 36 | 1092 | 70 | 82 | 101 | 5946 |
T. parva (AB499089) | 94 | 1440 | 642 | 301 | 111 | 38 | 38 | 1092 | 68 | 82 | 94 | 5924 |
T. orientalis (AB499090) | 47 | 1437 | 642 | 310 | 111 | 38 | 38 | 1092 | 69 | 82 | 47 | 5957 |
T. luwenshuni (MZ231018) | 123 | 1458 | 636 | 299 | 111 | 38 | 37 | 1092 | 69 | 82 | 123 | 6000 |
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Ulucesme, M.C.; Aktas, M.; Ozubek, S. Mitochondrial Genome Analysis of Babesia ovis (Apicomplexa: Babesiidae) Endemic in Sheep in Türkiye. Vet. Sci. 2024, 11, 554. https://doi.org/10.3390/vetsci11110554
Ulucesme MC, Aktas M, Ozubek S. Mitochondrial Genome Analysis of Babesia ovis (Apicomplexa: Babesiidae) Endemic in Sheep in Türkiye. Veterinary Sciences. 2024; 11(11):554. https://doi.org/10.3390/vetsci11110554
Chicago/Turabian StyleUlucesme, Mehmet Can, Munir Aktas, and Sezayi Ozubek. 2024. "Mitochondrial Genome Analysis of Babesia ovis (Apicomplexa: Babesiidae) Endemic in Sheep in Türkiye" Veterinary Sciences 11, no. 11: 554. https://doi.org/10.3390/vetsci11110554