Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-30T02:53:15.669Z Has data issue: false hasContentIssue false

Characterisation of the mitochondrial genome and phylogenetic analysis of Toxocara apodemi (Nematoda: Ascarididae)

Published online by Cambridge University Press:  15 April 2024

Y. Gao
Affiliation:
Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou Key Laboratory of Biomedicine and Advanced Dosage Forms, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China Zhejiang-Malaysia Joint Laboratory for Bioactive Materials and Applied Microbiology, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China
Y. Hu
Affiliation:
Taizhou City Center for Disease Control and Prevention, Zhejiang Taizhou 318000, China
S. Xu
Affiliation:
Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou Key Laboratory of Biomedicine and Advanced Dosage Forms, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China Zhejiang-Malaysia Joint Laboratory for Bioactive Materials and Applied Microbiology, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China
H. Liang
Affiliation:
Taizhou City Center for Disease Control and Prevention, Zhejiang Taizhou 318000, China
H. Lin
Affiliation:
Taizhou City Center for Disease Control and Prevention, Zhejiang Taizhou 318000, China
T. H. Yin
Affiliation:
Zhejiang-Malaysia Joint Laboratory for Bioactive Materials and Applied Microbiology, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China Tunku Abdul Rahman University of Management and Technology, Jalan Genting Kelang, Kuala Lumpur 53300, Malaysia
K. Zhao*
Affiliation:
Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou Key Laboratory of Biomedicine and Advanced Dosage Forms, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China Zhejiang-Malaysia Joint Laboratory for Bioactive Materials and Applied Microbiology, School of Life Sciences, Taizhou University, Zhejiang Taizhou 318000, China
*
Corresponding author: K. Zhao; Email: zybin395@126.com

Abstract

We first sequenced and characterised the complete mitochondrial genome of Toxocara apodeme, then studied the evolutionary relationship of the species within Toxocaridae. The complete mitochondrial genome was amplified using PCR with 14 specific primers. The mitogenome length was 14303 bp in size, including 12 PCGs (encoding 3,423 amino acids), 22 tRNAs, 2 rRNAs, and 2 NCRs, with 68.38% A+T contents. The mt genomes of T. apodemi had relatively compact structures with 11 intergenic spacers and 5 overlaps. Comparative analyses of the nucleotide sequences of complete mt genomes showed that T. apodemi had higher identities with T. canis than other congeners. A sliding window analysis of 12 PCGs among 5 Toxocara species indicated that nad4 had the highest sequence divergence, and cox1 was the least variable gene. Relative synonymous codon usage showed that UUG, ACU, CCU, CGU, and UCU most frequently occurred in the complete genomes of T. apodemi. The Ka/Ks ratio showed that all Toxocara mt genes were subject to purification selection. The largest genetic distance between T. apodemi and the other 4 congeneric species was found in nad2, and the smallest was found in cox2. Phylogenetic analyses based on the concatenated amino acid sequences of 12 PCGs demonstrated that T. apodemi formed a distinct branch and was always a sister taxon to other congeneric species. The present study determined the complete mt genome sequences of T. apodemi, which provide novel genetic markers for further studies of the taxonomy, population genetics, and systematics of the Toxocaridae nematodes.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Asakawa, M, Li, JF, Guo, A, Yang, X, Huhebateer Liu, ZL, Liu, YL, Cao, X, Chen, K (1994). A new host and locality record for Toxocara apodemi (Olsen, 1957) (Nematoda:Ascarididae) from striped field mice, Apodemus agrarius (pallas) (Rodentia:Murinae) in Changsha, ChinaJournal of Rakuno Gakuen University Natural Science 19, 193196.Google Scholar
Burland, TG (2000). DNASTAR’s Lasergene sequence analysis software. Methods in Molecular Biology 132, 7191. https://doi.org/10.1385/1-59259-192-2:71Google ScholarPubMed
Chagas, ATA, Ludwig, S, Pimentel, JDSM, de Abreu, NL, Nunez-Rodriguez, DL, Leal, HG, Kalapothakis, E (2020). Use of complete mitochondrial genome sequences to identify barcoding markers for groups with low genetic distanceMitochondrial DNA Part A 31, 139146. https://doi.org/10.1080/24701394.2020.1748609CrossRefGoogle ScholarPubMed
Chen, SY, Qiu, QG, Mo, HL (2022). Molecular identification and phylogenetic analysis of Ascarids in wild animalsFrontiers in Veterinary Science 9, 891672. https://doi.org/10.3389/fvets.2022.891672CrossRefGoogle ScholarPubMed
Gao, JF, Zhang, XX, Wang, XX, Li, Q, Li, Y, Xu, WW, Gao, Y, Wang, CR (2019). According to mitochondrial DNA evidence, Parascaris equorum and Parascaris univalens may represent the same speciesJournal of Helminthology 93, 383388. https://doi.org/10.1017/S0022149X18000330CrossRefGoogle ScholarPubMed
Gao, Y, Zhang, Z, Wang, C, Zhao, K (2022). The mitochondrial genome of Cylicocyclus elongatus (Strongylida: Strongylidae) and its comparative analysis with other Cylicocyclus speciesAnimals 12, 1571. https://doi.org/10.3390/ani12121571CrossRefGoogle ScholarPubMed
Gasser, RB, Bott, NJ, Chilton, NB, Hunt, P, Beveridge, I (2008). Toward practical, DNA-based diagnostic methods for parasitic nematodes of livestock–bionomic and biotechnological implicationsBiotechnology Advances 26, 325334. https://doi.org/10.1016/j.biotechadv.2008.03.003CrossRefGoogle ScholarPubMed
Gu, XH, Guo, N, Chen, HX, Sitko, J, Li, LW, Guo, BQ, Li, L (2023). Mitogenomic phylogenies suggest the resurrection of the subfamily Porrocaecinae and provide insights into the systematics of the superfamily Ascaridoidea (Nematoda: Ascaridomorpha), with the description of a new species of PorrocaecumParasites & Vectors 16, 275. https://doi.org/10.1186/s13071-023-05889-9CrossRefGoogle ScholarPubMed
Han, L, Yang, Y, Li, H, Zhou, X, Zhou, M, Liu, T, Lu, Y, Wang, Q, Yang, S, Shi, M, Li, X, Du, S, Guan, C, Zhang, Y, Guo, W, Wang, J, Chai, H, Lan, T, Liu, H, Liu, Q, Sun, H, Hou, Z (2022). Gene rearrangements in the mitochondrial genome of ten ascaris species and phylogenetic implications for Ascaridoidea and Heterakoidea familiesInternational Journal of Biological Macromolecules 221, 13941403. https://doi.org/10.1016/j.ijbiomac.2022.08.021CrossRefGoogle ScholarPubMed
Jin, YC, Li, XY, Liu, JH, Zhu, XQ, Liu, GH (2019). Comparative analysis of mitochondrial DNA datasets indicates that Toxascaris leonina represents a species complexParasites & Vectors 12, 194. https://doi.org/10.1186/s13071-019-3447-2CrossRefGoogle ScholarPubMed
Jones, DT, Taylor, WR, Thornton, JM (1992). The rapid generation of mutation data matrices from protein sequencesBioinformatics 8, 275282. https://doi.org/10.1093/bioinformatics/8.3.275CrossRefGoogle ScholarPubMed
Katoh, K, Standley, DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4), 772780. https://doi.org/10.1093/molbev/mst010CrossRefGoogle ScholarPubMed
Kim, HC, Hong, EJ, Ryu, SY, Park, J, Cho, JG, Yu, DH, Chae, JS, Choi, KS, Park, BK (2020). Morphological and molecular characterization of Toxocara apodemi (Nematoda: Ascarididae) from Striped Field Mice, Apodemus agrarius, in KoreaThe Korean Journal of Parasitology 58, 403411. https://doi.org/10.3347/kjp.2020.58.4.403CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C, Tamura, K (2018). MEGA X: Molecular evolutionary genetics analysis across computing platformsMolecular Biology and Evolution 35, 15471549. https://doi.org/10.1093/molbev/msy096CrossRefGoogle ScholarPubMed
Li, MW, Lin, RQ, Song, HQ, Wu, XY, Zhu, XQ (2008). The complete mitochondrial genomes for three Toxocara species of human and animal health significanceBMC Genomics 9, 224. https://doi.org/10.1186/1471-2164-9-224CrossRefGoogle ScholarPubMed
Librado, P, Rozas, J (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism dataBioinformatics 25, 14511452. https://doi.org/10.1093/bioinformatics/btp187CrossRefGoogle ScholarPubMed
Liu, GH, Wu, CY, Song, HQ, Wei, SJ, Xu, MJ, Lin, RQ, Zhao, GH, Huang, SY, Zhu, XQ (2012). Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigsGene 492, 110116. https://doi.org/10.1016/j.gene.2011.10.043CrossRefGoogle ScholarPubMed
Liu, GH, Shao, R, Li, JY, Zhou, DH, Li, H, Zhu, XQ (2013a). The complete mitochondrial genomes of three parasitic nematodes of birds: A unique gene order and insights into nematode phylogenyBMC Genomics 14, 414. https://doi.org/10.1186/1471-2164-14-414CrossRefGoogle ScholarPubMed
Liu, GH, Gasser, RB, Otranto, D, Xu, MJ, Shen, JL, Mohandas, N, Zhou, DH, Zhu, XQ (2013b). Mitochondrial genome of the eyeworm, Thelazia callipaeda (Nematoda: Spirurida), as the first representative from the family ThelaziidaePLoS Neglected Tropical Diseases 7(1), e2029. https://doi.org/10.1371/journal.pntd.0002029CrossRefGoogle ScholarPubMed
Liu, GH, Nadler, SA, Liu, SS, Podolska, M, D’Amelio, S, Shao, R, Gasser, RB, Zhu, XQ (2016). Mitochondrial phylogenomics yields strongly supported hypotheses for Ascaridomorph nematodesScientific Reports 6, 39248. https://doi.org/10.1038/srep39248CrossRefGoogle ScholarPubMed
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ, Higgins, DG (2007). Clustal W and Clustal X version 2.0Bioinformatics 23, 29472948. https://doi.org/10.1093/bioinformatics/btm404CrossRefGoogle ScholarPubMed
Meng, X, Xie, Y, Gu, X, Zheng, Y, Liu, Y, Li, Y, Wang, L, Zhou, X, Zuo, Z, Yang, G (2019). Sequencing and analysis of the complete mitochondrial genome of dog roundworm Toxocara canis (Nematoda: Toxocaridae) from USAMitochondrial DNA Part B 4, 29993001. https://doi.org/10.1080/23802359.2019.1666042CrossRefGoogle ScholarPubMed
Okimoto, R, Macfarlane, JL, Clary, DO, Wolstenholme, DR (1992). The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471498. https://doi.org/10.1093/genetics/130.3.471Google ScholarPubMed
Olsen, LS (1957). A new species of Neoascaris (Nematoda) from a Korean wood mouse. Transactions of the American Microscopical Society 2, 205208.CrossRefGoogle Scholar
Ronquist, F, Huelsenbeck, JP (2003). MrBayes 3: Bayesian phylogenetic inference under mixed modelsBioinformatics 19, 15721574. https://doi.org/10.1093/bioinformatics/btg180CrossRefGoogle ScholarPubMed
Warren, EG (1972). Two new species of Toxocara from viverrid hostsParasitology 65, 179187. https://doi.org/10.1017/s0031182000044978CrossRefGoogle ScholarPubMed
Xie, Y, Zhang, Z, Wang, C, Lan, J, Li, Y, Chen, Z, Fu, Y, Nie, H, Yan, N, Gu, X, Wang, S, Peng, X, Yang, G (2011). Complete mitochondrial genomes of Baylisascaris schroederi, Baylisascaris ailuri and Baylisascaris transfuga from giant panda, red panda and polar bearGene 482, 5967. https://doi.org/10.1016/j.gene.2011.05.004CrossRefGoogle ScholarPubMed
Xie, Y, Wang, L, Chen, Y, Wang, Z, Zhu, P, Hu, Z, Han, X, Wang, Z, Zhou, X, Zuo, Z (2022). The complete mitogenome of Toxocara vitulorum: Novel in-sights into the phylogenetics in ToxocaridaeAnimals 12, 3546. https://doi.org/10.3390/ani12243546CrossRefGoogle ScholarPubMed
Xing, ZP, Liang, X, Wang, X, Hu, HY, Huang, YX (2022). Novel gene rearrangement pattern in mitochondrial genome of Ooencyrtusplautus Huang & Noyes, 1994: New gene order in Encyrtidae (Hymenoptera, Chalcidoidea)ZooKeys 1124, 121. https://doi.org/10.3897/zookeys.1124.83811CrossRefGoogle ScholarPubMed
Yang, J, Huang, X, Wang, Y, Yang, H, Zhang, X, Zheng, X (2023). Complete mitogenome of Nycteribia allotopa Speiser, 1901 (Diptera, Hippoboscoidea, Nycteribiidae) and comparative analysis of mitochondrial genomes of NycteribiidaeParasitology International 96, 102769. https://doi.org/10.1016/j.parint.2023.102769CrossRefGoogle ScholarPubMed
Zhou, C, Guo, T, Deng, Y, He, J, Ouyang, S, Wu, X (2020). Mitochondrial phylogenomics of human-type Ascaris, pig-type Ascaris, and hybrid Ascaris populationsVeterinary Parasitology 287, 109256. https://doi.org/10.1016/j.vetpar.2020.109256CrossRefGoogle ScholarPubMed
Zhou, CY, Ma, J, Tang, QW, Zhu, XQ, Xu, QM (2021). The mitogenome of Ophidascaris wangi isolated from snakes in ChinaParasitology Research 120, 16771686. https://doi.org/10.1007/s00436-021-07069-zCrossRefGoogle ScholarPubMed
Ziegler, MA, Macpherson, CNL (2019). Toxocara and its species. CAB Reviews 14, 53.Google Scholar
Supplementary material: File

Gao et al. supplementary material 1

Gao et al. supplementary material
Download Gao et al. supplementary material 1(File)
File 11.4 MB
Supplementary material: File

Gao et al. supplementary material 2

Gao et al. supplementary material
Download Gao et al. supplementary material 2(File)
File 76.5 KB
Supplementary material: File

Gao et al. supplementary material 3

Gao et al. supplementary material
Download Gao et al. supplementary material 3(File)
File 49.7 KB
Supplementary material: File

Gao et al. supplementary material 4

Gao et al. supplementary material
Download Gao et al. supplementary material 4(File)
File 16.4 KB