Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes

Mitochondrial genomes are known for their compact size and conserved gene order, however, recent studies employing long-read sequencing technologies have revealed the presence of atypical mitogenomes in some species. In this study, we assembled and annotated the mitogenomes of five Antarctic notothe...

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Published in:Scientific Reports
Main Authors: Minhas, Bushra Fazal, Beck, Emily A., Cheng, C.-H. Christina, Catchen, Julian
Format: Text
Language:English
Published: Nature Publishing Group UK 2023
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10147917/
http://www.ncbi.nlm.nih.gov/pubmed/37117267
https://doi.org/10.1038/s41598-023-34237-1
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10147917 2023-06-11T04:07:01+02:00 Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes Minhas, Bushra Fazal Beck, Emily A. Cheng, C.-H. Christina Catchen, Julian 2023-04-28 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10147917/ http://www.ncbi.nlm.nih.gov/pubmed/37117267 https://doi.org/10.1038/s41598-023-34237-1 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10147917/ http://www.ncbi.nlm.nih.gov/pubmed/37117267 http://dx.doi.org/10.1038/s41598-023-34237-1 © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/) . Sci Rep Article Text 2023 ftpubmed https://doi.org/10.1038/s41598-023-34237-1 2023-05-07T01:03:05Z Mitochondrial genomes are known for their compact size and conserved gene order, however, recent studies employing long-read sequencing technologies have revealed the presence of atypical mitogenomes in some species. In this study, we assembled and annotated the mitogenomes of five Antarctic notothenioids, including four icefishes (Champsocephalus gunnari, C. esox, Chaenocephalus aceratus, and Pseudochaenichthys georgianus) and the cold-specialized Trematomus borchgrevinki. Antarctic notothenioids are known to harbor some rearrangements in their mt genomes, however the extensive duplications in icefishes observed in our study have never been reported before. In the icefishes, we observed duplications of the protein coding gene ND6, two transfer RNAs, and the control region with different copy number variants present within the same individuals and with some ND6 duplications appearing to follow the canonical Duplication-Degeneration-Complementation (DDC) model in C. esox and C. gunnari. In addition, using long-read sequencing and k-mer analysis, we were able to detect extensive heteroplasmy in C. aceratus and C. esox. We also observed a large inversion in the mitogenome of T. borchgrevinki, along with the presence of tandem repeats in its control region. This study is the first in using long-read sequencing to assemble and identify structural variants and heteroplasmy in notothenioid mitogenomes and signifies the importance of long-reads in resolving complex mitochondrial architectures. Identification of such wide-ranging structural variants in the mitogenomes of these fishes could provide insight into the genetic basis of the atypical icefish mitochondrial physiology and more generally may provide insights about their potential role in cold adaptation. Text Antarc* Antarctic Icefish PubMed Central (PMC) Antarctic Scientific Reports 13 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Article
spellingShingle Article
Minhas, Bushra Fazal
Beck, Emily A.
Cheng, C.-H. Christina
Catchen, Julian
Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
topic_facet Article
description Mitochondrial genomes are known for their compact size and conserved gene order, however, recent studies employing long-read sequencing technologies have revealed the presence of atypical mitogenomes in some species. In this study, we assembled and annotated the mitogenomes of five Antarctic notothenioids, including four icefishes (Champsocephalus gunnari, C. esox, Chaenocephalus aceratus, and Pseudochaenichthys georgianus) and the cold-specialized Trematomus borchgrevinki. Antarctic notothenioids are known to harbor some rearrangements in their mt genomes, however the extensive duplications in icefishes observed in our study have never been reported before. In the icefishes, we observed duplications of the protein coding gene ND6, two transfer RNAs, and the control region with different copy number variants present within the same individuals and with some ND6 duplications appearing to follow the canonical Duplication-Degeneration-Complementation (DDC) model in C. esox and C. gunnari. In addition, using long-read sequencing and k-mer analysis, we were able to detect extensive heteroplasmy in C. aceratus and C. esox. We also observed a large inversion in the mitogenome of T. borchgrevinki, along with the presence of tandem repeats in its control region. This study is the first in using long-read sequencing to assemble and identify structural variants and heteroplasmy in notothenioid mitogenomes and signifies the importance of long-reads in resolving complex mitochondrial architectures. Identification of such wide-ranging structural variants in the mitogenomes of these fishes could provide insight into the genetic basis of the atypical icefish mitochondrial physiology and more generally may provide insights about their potential role in cold adaptation.
format Text
author Minhas, Bushra Fazal
Beck, Emily A.
Cheng, C.-H. Christina
Catchen, Julian
author_facet Minhas, Bushra Fazal
Beck, Emily A.
Cheng, C.-H. Christina
Catchen, Julian
author_sort Minhas, Bushra Fazal
title Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
title_short Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
title_full Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
title_fullStr Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
title_full_unstemmed Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes
title_sort novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in antarctic notothenioid fishes
publisher Nature Publishing Group UK
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10147917/
http://www.ncbi.nlm.nih.gov/pubmed/37117267
https://doi.org/10.1038/s41598-023-34237-1
geographic Antarctic
geographic_facet Antarctic
genre Antarc*
Antarctic
Icefish
genre_facet Antarc*
Antarctic
Icefish
op_source Sci Rep
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10147917/
http://www.ncbi.nlm.nih.gov/pubmed/37117267
http://dx.doi.org/10.1038/s41598-023-34237-1
op_rights © The Author(s) 2023
https://creativecommons.org/licenses/by/4.0/Open Access This 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/) .
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