Mitophylogenomics of the zoonotic fluke Echinostoma malayanum confirms it as a member of the genus Artyfechinostomum Lane, 1915 and illustrates the complexity of Echinostomatidae systematics

Linh Thi Khanh Pham; Weerachai Saijuntha; Scott P Lawton; Thanh Hoa Le

doi:10.1007/s00436-022-07449-z

Mitophylogenomics of the zoonotic fluke Echinostoma malayanum confirms it as a member of the genus Artyfechinostomum Lane, 1915 and illustrates the complexity of Echinostomatidae systematics

Parasitol Res. 2022 Mar;121(3):899-913. doi: 10.1007/s00436-022-07449-z. Epub 2022 Feb 10.

Authors

Linh Thi Khanh Pham^{1

2}, Weerachai Saijuntha³, Scott P Lawton⁴, Thanh Hoa Le^{5

6}

Affiliations

¹ Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet Rd., Cau Giay, Hanoi, Vietnam.
² University of Science and Technology of Hanoi (USTH), Hanoi, Vietnam.
³ Walai Rukhavej Botanical Research Institute (WRBRI), Biodiversity and Conservation Research Unit, Mahasarakham University, Kham Riang, 44150, Mahasarakham, Thailand.
⁴ Department of Veterinary and Animal Sciences, Northern Faculty, Scotland's Rural College, An Lóchran, 10 Inverness Campus, Inverness, IV2 5NA, UK.
⁵ Immunology Department, Institute of Biotechnology (IBT), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet Rd., Cau Giay, Hanoi, Vietnam. imibtvn@gmail.com.
⁶ Graduate University of Science and Technology (GUST), Vietnam Academy of Science and Technology (VAST), 18. Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam. imibtvn@gmail.com.

PMID: 35142926
DOI: 10.1007/s00436-022-07449-z

Abstract

The complete mitochondrial genome (mitogenome or mtDNA) of the trematode Echinostoma malayanum Leiper, 1911 was fully determined and annotated. The circular mtDNA molecule comprised 12 protein-coding genes (PCGs) (cox1 - 3, cob, nad1 - 6, nad4L, atp6), two mitoribosomal RNAs (MRGs) (16S or rrnL and 12S or rrnS), and 22 transfer RNAs (tRNAs or trn), and a non-coding region (NCR) rich in long and short tandem repeats (5.5 LRUs/336 bp/each and 7.5 SRUs/207 bp/each). The atp8 gene is absent and the 3' end of nad4L overlaps the 5' end of nad4 by 40 bp. Special DHU-arm missing tRNAs for Serine were found for both tRNA^Ser1(AGN) and tRNA^Ser2(UCN). Codons of TTT (for phenylalanine), TTG (for leucine), and GTT (for valine) were the most, and CGC (for Arginine) was the least frequently used. A similar usage pattern was seen in base composition, AT and GC skewness for PCGs, MRGs, and mtDNA* (coding cox3 to nad5) in E. malayanum and Echinostomatidae. The nucleotide use is characterized by (T > G > A > C) for PCGs/mtDNA*, and by (T > G ≈ A > C) for MRGs. E. malayanum exhibited the lowest genetic distance (0.53%) to Artyfechinostomum sufrartyfex, relatively high to the Echinostoma congeners (13.20-13.99%), higher to Hypoderaeum conoideum (16.18%), and the highest to interfamilial Echinochasmidae (26.62%); Cyclocoelidae (30.24%); and Himasthlidae (25.36%). Topology indicated the monophyletic position between E. malayanum/A. sufrartyfex and the group of Echinostoma caproni, Echinostoma paraensei, Echinostoma miyagawai, and Echinostoma revolutum, rendering Hypoderaeum conoideum and unidentified Echinostoma species paraphyletic. The strictly closed genomic/taxonomic/phylogenetic features (including base composition, skewness, codon usage/bias, genetic distance, and topo-position) reinforced Echinostoma malayanum to retake its generic validity within the Artyfechinostomum genus.

Keywords: Echinostoma/Artyfechinostomum malayanum; Echinostomata; Echinostomatidae; Genetic distance; Mitophylogenetics; Skewness; Tandem repeats.

MeSH terms

Animals
Echinostoma* / genetics
Echinostomatidae* / genetics
Genome, Mitochondrial*
Phylogeny
Trematoda* / genetics

Grants and funding

108.02-2020.07/NAFOSTED