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Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin

BACKGROUND: Raillietina species belong to the family Davaineidae, which parasitizes in a wide variety of mammals and birds, causing stunted growth, lethargy, emaciation, and digestive tract obstruction. However, only a limited number of Raillietina species have been identified in wild animals. METHO...

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Autores principales: Tuli, Merga Daba, Li, Hongyi, Pan, Xi, Li, Song, Zhai, Junqiong, Wu, Yajiang, Chen, Wu, Huang, Wanyi, Feng, Yaoyu, Xiao, Lihua, Yuan, Dongjuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195439/
https://www.ncbi.nlm.nih.gov/pubmed/35698206
http://dx.doi.org/10.1186/s13071-022-05301-y
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author Tuli, Merga Daba
Li, Hongyi
Pan, Xi
Li, Song
Zhai, Junqiong
Wu, Yajiang
Chen, Wu
Huang, Wanyi
Feng, Yaoyu
Xiao, Lihua
Yuan, Dongjuan
author_facet Tuli, Merga Daba
Li, Hongyi
Pan, Xi
Li, Song
Zhai, Junqiong
Wu, Yajiang
Chen, Wu
Huang, Wanyi
Feng, Yaoyu
Xiao, Lihua
Yuan, Dongjuan
author_sort Tuli, Merga Daba
collection PubMed
description BACKGROUND: Raillietina species belong to the family Davaineidae, which parasitizes in a wide variety of mammals and birds, causing stunted growth, lethargy, emaciation, and digestive tract obstruction. However, only a limited number of Raillietina species have been identified in wild animals. METHODS: We analyzed and annotated the complete mitochondrial (mt) genome of a worm from the intestine of a wild pangolin using Illumina sequencing of whole genomic DNA. RESULTS: These findings showed the presence of two mtDNA sequences in Raillietina sp., designated as mt1 and mt2, with the lengths of 14,331 bp and 14,341 bp, respectively. Both the mts genomes of Raillietina sp. comprised 36 genes, containing 12 protein-coding genes (PCGs), 2 ribosomal RNAs, and 22 transfer RNAs. Gene arrangements of both mt genomes of Raillietina sp. were similar to those of most flatworms, except for taeniids, which shift positions between tRNAL1 and tRNAS2 genes. Twenty of 22 tRNA secondary structures of Raillietina sp. had a typical cloverleaf structure similar to Raillietina tetragona. Sequence differences between the mt1 and mt2 genomes were 4.4%, and this difference arises from the mtDNA heteroplasmic mutations. Moreover, heteroplasmic mtDNA mutations were detected in PCGs, tRNAs, rRNAs, NCRs, and intergenes, but the highest proportion of heteroplasmy of 79.0% was detected in PCGs, indicating the occurrence of mtDNA heteroplasmy in Raillietina sp. To our knowledge, this is the first report of mtDNA heteroplasmy in tapeworm parasites. Phylogenetic analyses of 18S rRNA, ITS2, and 12 PCG sequences demonstrated that the worm was clustered with other Raillietina species in the Davaneidae family. CONCLUSIONS: We found a novel Raillietina species in wild pangolin with the existence of mitochondrial DNA heteroplasmy. Thus, these findings provide insights into the heterogeneity of the mt genome in parasitic cestodes, and mt genome data contributes to the understanding of pangolin-parasitic cestodes in terms of their molecular biology, epidemiology, diagnosis, and taxonomy. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05301-y.
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spelling pubmed-91954392022-06-15 Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin Tuli, Merga Daba Li, Hongyi Pan, Xi Li, Song Zhai, Junqiong Wu, Yajiang Chen, Wu Huang, Wanyi Feng, Yaoyu Xiao, Lihua Yuan, Dongjuan Parasit Vectors Research BACKGROUND: Raillietina species belong to the family Davaineidae, which parasitizes in a wide variety of mammals and birds, causing stunted growth, lethargy, emaciation, and digestive tract obstruction. However, only a limited number of Raillietina species have been identified in wild animals. METHODS: We analyzed and annotated the complete mitochondrial (mt) genome of a worm from the intestine of a wild pangolin using Illumina sequencing of whole genomic DNA. RESULTS: These findings showed the presence of two mtDNA sequences in Raillietina sp., designated as mt1 and mt2, with the lengths of 14,331 bp and 14,341 bp, respectively. Both the mts genomes of Raillietina sp. comprised 36 genes, containing 12 protein-coding genes (PCGs), 2 ribosomal RNAs, and 22 transfer RNAs. Gene arrangements of both mt genomes of Raillietina sp. were similar to those of most flatworms, except for taeniids, which shift positions between tRNAL1 and tRNAS2 genes. Twenty of 22 tRNA secondary structures of Raillietina sp. had a typical cloverleaf structure similar to Raillietina tetragona. Sequence differences between the mt1 and mt2 genomes were 4.4%, and this difference arises from the mtDNA heteroplasmic mutations. Moreover, heteroplasmic mtDNA mutations were detected in PCGs, tRNAs, rRNAs, NCRs, and intergenes, but the highest proportion of heteroplasmy of 79.0% was detected in PCGs, indicating the occurrence of mtDNA heteroplasmy in Raillietina sp. To our knowledge, this is the first report of mtDNA heteroplasmy in tapeworm parasites. Phylogenetic analyses of 18S rRNA, ITS2, and 12 PCG sequences demonstrated that the worm was clustered with other Raillietina species in the Davaneidae family. CONCLUSIONS: We found a novel Raillietina species in wild pangolin with the existence of mitochondrial DNA heteroplasmy. Thus, these findings provide insights into the heterogeneity of the mt genome in parasitic cestodes, and mt genome data contributes to the understanding of pangolin-parasitic cestodes in terms of their molecular biology, epidemiology, diagnosis, and taxonomy. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05301-y. BioMed Central 2022-06-13 /pmc/articles/PMC9195439/ /pubmed/35698206 http://dx.doi.org/10.1186/s13071-022-05301-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Tuli, Merga Daba
Li, Hongyi
Pan, Xi
Li, Song
Zhai, Junqiong
Wu, Yajiang
Chen, Wu
Huang, Wanyi
Feng, Yaoyu
Xiao, Lihua
Yuan, Dongjuan
Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title_full Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title_fullStr Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title_full_unstemmed Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title_short Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild Pangolin
title_sort heteroplasmic mitochondrial genomes of a raillietina tapeworm in wild pangolin
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195439/
https://www.ncbi.nlm.nih.gov/pubmed/35698206
http://dx.doi.org/10.1186/s13071-022-05301-y
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