Skip to main content

Characterization of the complete mitochondrial genome of the echinostome Echinostoma miyagawai and phylogenetic implications

Parasitology Research volume 118, pages 3091–3097 (2019)Cite this article

Abstract

Echinostomes are important intestinal foodborne parasites. Despite their significance as pathogens, characterization of the molecular biology and phylogenetics of these parasites are limited. In the present study, we determined the entire mitochondrial (mt) genome of the echinostome Echinostoma miyagawai (Hunan isolate) and examined the phylogenetic relationship with selected members of the suborder Echinostomata. The complete mt genome of E. miyagawai (Hunan isolate) was 14,468 bp in size. This circular mt genome contained 12 protein-coding genes, 22 transfer RNA genes, two ribosomal RNA genes, and one non-coding region. The gene order and genomic content were identical with its congeners. Phylogenetic analyses (maximum parsimony, maximum likelihood, and Bayesian inference) based on the concatenated amino acid sequences of 12 protein-coding genes strongly supported monophyly for the genus Echinostoma; however, they rejected monophyly for the family Echinostomatidae and the genus Fasciola. The mt genomic data described in this study provides useful genetic markers for studying the population genetics, molecular biology, and phylogenetics of these echinostomes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Buddhachat K, Chontananarth (2019) Is species identification of Echinostoma revolutum using mitochondrial DNA barcoding feasible with high-resolution melting analysis? Parasitol Res 118:1799–1810

    Article  PubMed  Google Scholar 

  • Cai XQ, Liu GH, Song HQ, Wu CY, Zou FC, Yan HK, Yuan ZG, Lin RQ, Zhu XQ (2012) Sequences and gene organization of the mitochondrial genomes of the liver flukes Opisthorchis viverrini and Clonorchis sinensis (Trematoda). Parasitol Res 110:235–243

    Article  CAS  PubMed  Google Scholar 

  • Detwiler JT, Bos DH, Minchella DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Mol Phylogenet Evol 55:611–620

    Article  PubMed  Google Scholar 

  • Gasser RB (2006) Molecular tools—advances, opportunities and prospects. Vet Parasitol 136:69–89

    Article  CAS  PubMed  Google Scholar 

  • Georgieva S, Faltýnková A, Brown R, Blasco-Costa I, Soldánová M, Sitko J, Scholz T, Kostadinova A (2014) Echinostoma ‘revolutum’ (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasit Vectors 7:520

    PubMed  PubMed Central  Google Scholar 

  • Graczyk TK, Fried B (1998) Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg 58:501–504

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

  • Kostadinova A, Herniou EA, Barrett J, Littlewood DT (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176

    Article  CAS  PubMed  Google Scholar 

  • Le TH, Blair D, McManus DP (2000) Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Trop 77:243–256

    Article  CAS  PubMed  Google Scholar 

  • Le TH, Nguyen NTB, Nguyen KT, Doan HTT, Dung DT, Blair D (2016) A complete mitochondrial genome from Echinochasmus japonicus supports the elevation of Echinochasminae Odhner, 1910 to family rank (Trematoda: Platyhelminthes). Infect Genet Evol 45:369–377

    Article  CAS  PubMed  Google Scholar 

  • Liu GH, Yan HB, Otranto D, Wang XY, Zhao GH, Jia WZ, Zhu XQ (2014) Dicrocoelium chinensis and Dicrocoelium dendriticum (Trematoda: Digenea) are distinct lancet fluke species based on mitochondrial and nuclear ribosomal DNA sequences. Mol Phylogenet Evol 79:325–331

    Article  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, He JJ, Liu GH, Leontovyč R, Kašný M, Zhu XQ (2016) Complete mitochondrial genome of the giant liver fluke Fascioloides magna (Digenea: Fasciolidae) and its comparison with selected trematodes. Parasit Vectors 9:429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Sun MM, He JJ, Liu GH, Ai L, Chen MX, Zhu XQ (2017) Fasciolopsis buski (Digenea: Fasciolidae) from China and India may represent distinct taxa based on mitochondrial and nuclear ribosomal DNA sequences. Parasit Vectors 10:101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanta UK, Watanabe T, Anisuzzaman OY, Itagaki T (2019) Characterization of Echinostoma revolutum and Echinostoma robustum from ducks in Bangladesh based on morphology, nuclear ribosomal ITS2 and mitochondrial nad1 sequences. Parasitol Int 69:1–7

    Article  CAS  PubMed  Google Scholar 

  • Na L, Gao JF, Liu GH, Fu X, Su X, Yue DM, Gao Y, Zhang Y, Wang CR (2016) The complete mitochondrial genome of Metorchis orientalis (Trematoda: Opisthorchiidae): comparison with other closely related species and phylogenetic implications. Infect Genet Evol 39:45–50

    Article  CAS  PubMed  Google Scholar 

  • Nagataki M, Tantrawatpan C, Agatsuma T, Sugiura T, Duenngai K, Sithithaworn P, Andrews RH, Petney TN, Saijuntha W (2015) Mitochondrial DNA sequences of 37 collar-spined echinostomes (Digenea: Echinostomatidae) in Thailand and Lao PDR reveals presence of two species: Echinostoma revolutum and E. miyagawai. Infect Genet Evol 35:56–62

    Article  CAS  PubMed  Google Scholar 

  • Noikong W, Wongsawad C, Chai JY, Saenphet S, Trudgett A (2014) Molecular analysis of echinostome metacercariae from their second intermediate host found in a localised geographic region reveals genetic heterogeneity and possible cryptic speciation. PLoS Negl Trop Dis 8: 2778

  • Platt TR, Zelmer DA (2016) Effect of infection duration on habitat selection and morphology of adult Echinostoma caproni (Digenea: Echinostomatidae) in ICR mice. J Parasitol 102:37–41

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saijuntha W, Sithithaworn P, Duenngai K, Kiatsopit N, Andrews RH, Petney TN (2011) Genetic variation and relationships of four species of medically important echinostomes (Trematoda: Echinostomatidae) in South-East Asia. Infect Genet Evol 11:375–381

    Article  PubMed  Google Scholar 

  • Shin EH, Guk SM, Kim HJ, Lee SH, Chai JY (2008) Trends in parasitic diseases in the Republic of Korea. Trends Parasitol 24:143–150

    Article  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  • Toledo R, Radev V, Kanev I, Gardner SL, Fried B (2014) History of echinostomes (Trematoda). Acta Parasitol 59:555–567

    Article  PubMed  Google Scholar 

  • Toledo R, Esteban JG (2016) An update on human echinostomiasis. Trans R Soc Trop Med Hyg 110:37–45

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Wang L, Chen H, Feng H, Shen B, Hu M, Fang R (2016) The complete mitochondrial genome of Gastrothylax crumenifer (Gastrothylacidae, Trematoda) and comparative analyses with selected trematodes. Parasitol Res 115:2489–2497

    Article  PubMed  Google Scholar 

  • Zhang D, Li WX, Zou H, Wu SG, Li M, Jakovlić I, Zhang J, Chen R, Wang GT (2018) Mitochondrial genomes of two diplectanids (Platyhelminthes: Monogenea) expose paraphyly of the order Dactylogyridea and extensive tRNA gene rearrangements. Parasit Vectors 11:601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was financially supported by the Planned Program of Hunan Province Science and Technology Innovation (Grant no. 2018RS3085) and the Training Program for Excellent Young Innovators of Changsha (Grant no. KQ1802035).

Author information

Affiliations

  1. Hunan Provincial Key Laboratory of Protein Engineering in Animal Vaccines, College of Veterinary Medicine, Hunan Agricultural University, Changsha, 410128, Hunan Province, China

    Yi-Tian Fu, Yuan-Chun Jin, Fen Li & Guo-Hua Liu

  2. Hunan Co-Innovation Center of Animal Production Safety, Changsha, 410128, Hunan Province, China

    Fen Li & Guo-Hua Liu

Authors
  1. Yi-Tian Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan-Chun Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guo-Hua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Fen Li or Guo-Hua Liu.

Ethics declarations

All procedures involving animals in the present study were approved, and this study was approved by the Animal Ethics Committee of Hunan Agricultural University (No. 43321503).

Competing interests

The authors declared that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Section Editor: Christoph G. Grevelding

Electronic supplementary material

Supplementary material S1
figure 3

Inferred phylogenetic relationship among representative Echinostoma spp. and other suborder Echinostomata trematodes based on mitochondrial cox1 sequences utilizing maximum parsimony (MP), maximum likelihood (ML), and Bayesian inference (BI) using Opisthorchis viverrini as an outgroup. (PNG 4053 kb)

Full size image

High Resolution Image (TIF 1344 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fu, YT., Jin, YC., Li, F. et al. Characterization of the complete mitochondrial genome of the echinostome Echinostoma miyagawai and phylogenetic implications. Parasitol Res 118, 3091–3097 (2019). https://doi.org/10.1007/s00436-019-06417-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06417-4

Keywords

  • Echinostome
  • Mitochondrial genome
  • Mitochondrial DNA
  • Phylogenetic analyses