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Comparative mitogenomics of the zoonotic parasite Echinostoma revolutum resolves taxonomic relationships within the ‘E. revolutum’ species group and the Echinostomata (Platyhelminthes: Digenea)

Published online by Cambridge University Press:  29 January 2020

Thanh Hoa Le Open the ORCID record for Thanh Hoa Le [Opens in a new window] ,
Linh Thi Khanh Pham ,
Huong Thi Thanh Doan ,
Xuyen Thi Kim Le ,
Weerachai Saijuntha ,
R.P.V. Jayanthe Rajapakse  and
Scott P. Lawton Open the ORCID record for Scott P. Lawton [Opens in a new window]
Thanh Hoa Le*
Affiliation:
Institute of Biotechnology (IBT); Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam Graduate University of Science and Technology (GUST), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam
Linh Thi Khanh Pham
Affiliation:
Institute of Biotechnology (IBT); Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam
Huong Thi Thanh Doan
Affiliation:
Institute of Biotechnology (IBT); Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam
Xuyen Thi Kim Le
Affiliation:
Institute of Biotechnology (IBT); Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet Rd, Cau Giay, Hanoi, Vietnam
Weerachai Saijuntha
Affiliation:
Walai Rukhavej Botanical Research Institute (WRBRI), Biodiversity and Conservation Research Unit, Mahasarakham University, Mahasarakham44150, Thailand
R.P.V. Jayanthe Rajapakse
Affiliation:
Department of Veterinary Pathobiology, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka
Scott P. Lawton
Affiliation:
Molecular Parasitology Laboratory, School of Life Sciences, Pharmacy and Chemistry, Kingston University London, Kingston Upon Thames, Surrey, KT1 2EE, UK
*
Author for correspondence: Thanh Hoa Le, E-mail: imibtvn@gmail.com
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Abstract

The complete mitochondrial sequence of 17,030 bp was obtained from Echinostoma revolutum and characterized with those of previously reported members of the superfamily Echinostomatoidea, i.e. six echinostomatids, one echinochasmid, five fasciolids, one himasthlid, and two cyclocoelids. Relationship within suborders and between superfamilies, such as Echinostomata, Pronocephalata, Troglotremata, Opisthorchiata, and Xiphiditata, are also considered. It contained 12 protein-coding, two ribosomal RNA, 22 transfer RNA genes and a tandem repetitive consisting non-coding region (NCR). The gene order, one way-positive transcription, the absence of atp8 and the overlapped region by 40 bp between nad4L and nad4 genes were similar as in common trematodes. The NCR located between tRNAGlu (trnE) and cox3 contained 11 long (LRUs) and short repeat units (SRUs) (seven LRUs of 317 bp, four SRUs of 207 bp each), and an internal spacer sequence between LRU7 and SRU4 specifying high-level polymorphism. Special DHU-arm missing tRNAs for Serine were found for both tRNAS1(AGN) and tRNAS2(UCN). Echinostoma revolutum indicated the lowest divergence rate to E. miyagawai and the highest to Tracheophilus cymbius and Echinochasmus japonicus. The usage of ATG/GTG start and TAG/TAA stop codons, the AT composition bias, the negative AT-skewness, and the most for Phe/Leu/Val and the least for Arg/Asn/Asp codons were noted. Topology indicated the monophyletic position of E. revolutum to E. miyagawai. Monophyly of Echinostomatidae and Fasciolidae was clearly solved with respect to Echinochasmidae, Himasthlidae, and Cyclocoelidae which were rendered paraphyletic in the suborder Echinostomata.

Keywords

‘37-collar-spined’Echinostoma revolutumEchinostomatidaeEchinostomatoideamitochondrial genomephylogenetic analysisrepeatsskewness value
Type
Research Article
Information
Parasitology , Volume 147 , Issue 5 , April 2020 , pp. 566 - 576
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Copyright
Copyright © Cambridge University Press 2020

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References

Benson, G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27, 573–580.CrossRefGoogle ScholarPubMed
Biswal, DK, Chatterjee, A, Bhattacharya, A and Tandon, V (2014) The mitochondrial genome of Paragonimus westermani (Kerbert, 1878), the Indian isolate of the lung fluke representative of the family Paragonimidae (Trematoda). Peer J 2, e484.CrossRefGoogle Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
Chai, JY (2009) Echinostomes in humans. In Fried, B and Toledo, R (eds), The Biology of Echinostomes. New York, USA: Springer, pp. 147–183.CrossRefGoogle Scholar
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
Faltýnková, A, Georgieva, S, Soldánová, M and Kostadinova, A (2015) A re-assessment of species diversity within the ‘revolutum’ group of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) in Europe. Systematic Parasitology 90, 1–25.CrossRefGoogle ScholarPubMed
Fu, YT, Jin, YC, Li, F and Liu, GH (2019) Characterization of the complete mitochondrial genome of the echinostome Echinostoma miyagawai and phylogenetic implications. Parasitology Research 118, 3091–3097.CrossRefGoogle ScholarPubMed
Gemayel, R, Vinces, MD, Legendre, M and Verstrepen, KJ (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics 44, 445–477.CrossRefGoogle ScholarPubMed
Georgieva, S, Selbach, C, Faltýnková, A, Soldánová, M, Sures, B, Skírnisson, K and Kostadinova, A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors 6, 64.CrossRefGoogle ScholarPubMed
Georgieva, S, Faltýnková, A, Brown, R, Blasco-Costa, I, Soldánová, M, Sitko, J, Scholz, T and Kostadinova, A (2014) Echinostoma ‘revolutum’ (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasites & Vectors 7, 520.Google ScholarPubMed
Gordy, MA and Hanington, PC (2019) A fine-scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution 9, 3153–3238.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kinkar, L, Korhonen, PK, Cai, H, Gauci, CG, Lightowlers, MW, Saarma, U, Jenkins, DJ, Li, J, Li, J, Young, ND and Gasser, RB (2019) Long-read sequencing reveals a 4.4 kb tandem repeat region in the mitogenome of Echinococcus granulosus (sensu stricto) genotype G1. Parasites & Vectors 12, 238.CrossRefGoogle ScholarPubMed
Kostadinova, A (2005) Family Echinostomatidae Looss, 1899. In Gibson, DI, Jones, A and Bray, AR (eds), Keys to the Trematoda, vol. 2, Wallingford: CAB International, pp. 9–64.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Laslett, D and Canback, B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics (Oxford, England) 24, 172–175.CrossRefGoogle ScholarPubMed
Le, TH, Blair, D and McManus, DP (2001) Complete DNA sequence and gene organization of the mitochondrial genome of the liver fluke, Fasciola hepatica L. (Platyhelminthes; Trematoda). Parasitology 123, 609–621.CrossRefGoogle Scholar
Le, TH, Blair, D and McManus, DP (2002) Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.CrossRefGoogle ScholarPubMed
Le, TH, Nguyen, NTB, Nguyen, KT, Doan, HTT, Dung, DT and Blair, D (2016) A complete mitochondrial genome from Echinochasmus japonicus supports the elevation of Echinochasminae Odhner, 1910 to family rank (Trematoda: Platyhelminthes). Infection, Genetics and Evolution 45, 369–377.CrossRefGoogle Scholar
Le, TH, Nguyen, KT, Nguyen, NTB, Doan, HTT, Agatsuma, T and Blair, D (2019) The complete mitochondrial genome of Paragonimus ohirai (Paragonimidae: Trematoda: Platyhelminthes) and its comparison with P. westermani Congeners and other trematodes. Peer J 7, e7031.CrossRefGoogle Scholar
Li, Y, Ma, XX, Lv, QB, Hu, Y, Qiu, HY, Chang, QC and Wang, CR (2019a) Characterization of the complete mitochondrial genome sequence of Tracheophilus cymbius (Digenea), the first representative from the family Cyclocoelidae. Journal of Helminthology 94, e101.CrossRefGoogle Scholar
Li, Y, Qiu, YY, Zeng, MH, Diao, PW, Chang, QC, Gao, Y, Zhang, Y and Wang, CR (2019b) The complete mitochondrial genome of Echinostoma miyagawai: comparisons with closely related species and phylogenetic implications. Infection, Genetics and Evolution 75, 103961.CrossRefGoogle Scholar
Littlewood, DT, Lockyer, AE, Webster, BL, Johnston, DA and Le, TH (2006) The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Molecular Phylogenetics and Evolution 39, 452–467.CrossRefGoogle ScholarPubMed
Liu, GH, Gasser, RB, Young, ND, Song, HQ, Ai, L and Zhu, XQ (2014) Complete mitochondrial genomes of the ‘intermediate form’ of Fasciola and Fasciola gigantica, and their comparison with F. hepatica. Parasites & Vectors 7, 150.CrossRefGoogle ScholarPubMed
Lowe, TM and Eddy, SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955–964.CrossRefGoogle ScholarPubMed
Lunt, DH, Whipple, LE and Hyman, BC (1998) Mitochondrial DNA variable number tandem repeats (VNTRs): utility and problems in molecular ecology. Molecular Ecology 7, 1441–1455.CrossRefGoogle ScholarPubMed
Ma, J, He, JJ, Liu, GH, Leontovyč, R, Kašný, M and Zhu, XQ (2016) Complete mitochondrial genome of the giant liver fluke Fascioloides magna (Digenea: Fasciolidae) and its comparison with selected trematodes. Parasites & Vectors 9, 429.CrossRefGoogle ScholarPubMed
Ma, J, Sun, MM, He, JJ, Liu, GH, Ai, L, Chen, MX and Zhu, XQ (2017) Fasciolopsis buski (Digenea: Fasciolidae) from China and India may represent distinct taxa based on mitochondrial and nuclear ribosomal DNA sequences. Parasites & Vectors 10, 101.CrossRefGoogle ScholarPubMed
Miliotis, MD and Bier, JW (2003) International Handbook of Foodborne Pathogens. New York: CRC Press.CrossRefGoogle Scholar
Nagataki, M, Tantrawatpan, C, Agatsuma, T, Sugiura, T, Duenngai, K, Sithithaworn, P, Andrews, RH, Petney, TN and 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. Infection, Genetics and Evolution 35, 56–62.CrossRefGoogle ScholarPubMed
Oey, H, Zakrzewski, M, Narain, K, Devi, KR, Agatsuma, T, Nawaratna, S, Gobert, GN, Jones, MK, Ragan, MA, McManus, DP and Krause, L (2019) Whole-genome sequence of the oriental lung fluke Paragonimus westermani. Gigascience 8, giy146.CrossRefGoogle ScholarPubMed
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle Scholar
Perna, NT and Kocher, TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353–358.CrossRefGoogle ScholarPubMed
Saijuntha, W, Sithithaworn, P, Duenngai, K, Kiatsopit, N, Andrews, RH and Petney, TN (2011a) Genetic variation and relationships of four species of medically important echinostomes (Trematoda: Echinostomatidae) in South-East Asia. Infection, Genetics and Evolution 11, 375–381.CrossRefGoogle Scholar
Saijuntha, W, Tantrawatpan, C, Sithithaworn, P, Andrews, RH and Petney, TN (2011b) Genetic characterization of Echinostoma revolutum and Echinoparyphium recurvatum (Trematoda: Echinostomatidae) in Thailand and phylogenetic relationships with other isolates inferred by ITS1 sequence. Parasitology Research 108, 751–755.CrossRefGoogle Scholar
Saijuntha, W, Tantrawatpan, C, Sithithaworn, P, Andrews, RH and Petney, TN (2011c) Spatial and temporal genetic variation of Echinostoma revolutum (Trematoda: Echinostomatidae) from Thailand and the Lao PDR. Acta Tropica 118, 105–109.CrossRefGoogle Scholar
Suleman, KM, Heneberg, P, Zhou, CY, Muhammad, N, Zhu, XQ and Ma, J (2019) Characterization of the complete mitochondrial genome of Uvitellina sp., representative of the family Cyclocoelidae and phylogenetic implications. Parasitology Research 118, 2203–2211.CrossRefGoogle ScholarPubMed
Tkach, VV, Kudlai, O and Kostadinova, A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171–185.CrossRefGoogle Scholar
Toledo, R and Esteban, JG (2016) An update on human echinostomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 37–45.CrossRefGoogle ScholarPubMed
Wey-Fabrizius, AR, Podsiadlowski, L, Herlyn, H and Hankeln, T (2013) Platyzoan mitochondrial genomes. Molecular Phylogenetics and Evolution 69, 365–375.CrossRefGoogle ScholarPubMed
Yang, X, Gasser, RB, Koehler, AV, Wang, L, Zhu, K, Chen, L, Feng, H, Hu, M and Fang, R (2015) Mitochondrial genome of Hypoderaeum conoideum – comparison with selected trematodes. Parasites & Vectors 8, 97.CrossRefGoogle ScholarPubMed
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