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

Linh Thi Khanh Pham, Weerachai Saijuntha, Scott P. Lawton, Thanh Hoa Le^*

^*Corresponding author for this work

Centre for Epidemiology and Planetary Health (CEPH)

Research output: Contribution to journal › Article › peer-review

7 Citations (Scopus)

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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.

Original language	English
Pages (from-to)	899-913
Number of pages	15
Journal	Parasitology Research
Volume	121
Issue number	3
Early online date	10 Feb 2022
DOIs	https://doi.org/10.1007/s00436-022-07449-z
Publication status	Print publication - Mar 2022

Bibliographical note

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Keywords

Echinostoma/Artyfechinostomum malayanum
Echinostomata
Echinostomatidae
Genetic distance
Mitophylogenetics
Skewness
Tandem repeats

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10.1007/s00436-022-07449-z

PARE-D-21-00945_R1 aamAccepted author manuscript, 1.7 MBLicence: CC BY

Cite this

@article{2713dcb62ccf41d3bb7dc6379f765686,

title = "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",

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 tRNASer1(AGN) and tRNASer2(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",

author = "Pham, {Linh Thi Khanh} and Weerachai Saijuntha and Lawton, {Scott P.} and Le, {Thanh Hoa}",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.",

year = "2022",

month = mar,

doi = "10.1007/s00436-022-07449-z",

language = "English",

volume = "121",

pages = "899--913",

journal = "Parasitology Research",

issn = "0932-0113",

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number = "3",

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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. / Pham, Linh Thi Khanh; Saijuntha, Weerachai; Lawton, Scott P. et al.
In: Parasitology Research, Vol. 121, No. 3, 03.2022, p. 899-913.

Research output: Contribution to journal › Article › peer-review

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AU - Pham, Linh Thi Khanh

AU - Saijuntha, Weerachai

AU - Lawton, Scott P.

AU - Le, Thanh Hoa

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AB - 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 tRNASer1(AGN) and tRNASer2(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.

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KW - Echinostomata

KW - Echinostomatidae

KW - Genetic distance

KW - Mitophylogenetics

KW - Skewness

KW - Tandem repeats

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ER -

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

Abstract

Bibliographical note

Keywords

UN SDGs

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