Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica

Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica isl...

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Published in:Communications Biology
Main Authors: Dégletagne, Cyril, Abele, Doris, Glöckner, Gernot, Alric, Benjamin, Gruber, Heike, Held, Christoph
Format: Text
Language:English
Published: Nature Publishing Group UK 2021
Subjects:
Article
Arctica islandica
Ocean quahog
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8452683/
http://www.ncbi.nlm.nih.gov/pubmed/34545198
https://doi.org/10.1038/s42003-021-02593-1
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spelling ftpubmed:oai:pubmedcentral.nih.gov:8452683 2023-05-15T15:22:30+02:00 Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica Dégletagne, Cyril Abele, Doris Glöckner, Gernot Alric, Benjamin Gruber, Heike Held, Christoph 2021-09-20 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8452683/ http://www.ncbi.nlm.nih.gov/pubmed/34545198 https://doi.org/10.1038/s42003-021-02593-1 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8452683/ http://www.ncbi.nlm.nih.gov/pubmed/34545198 http://dx.doi.org/10.1038/s42003-021-02593-1 © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . CC-BY Commun Biol Article Text 2021 ftpubmed https://doi.org/10.1038/s42003-021-02593-1 2021-10-10T00:25:01Z Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica, ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level. Text Arctica islandica Ocean quahog PubMed Central (PMC) Communications Biology 4 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Article
spellingShingle Article
Dégletagne, Cyril
Abele, Doris
Glöckner, Gernot
Alric, Benjamin
Gruber, Heike
Held, Christoph
Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
topic_facet Article
description Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica, ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level.
format Text
author Dégletagne, Cyril
Abele, Doris
Glöckner, Gernot
Alric, Benjamin
Gruber, Heike
Held, Christoph
author_facet Dégletagne, Cyril
Abele, Doris
Glöckner, Gernot
Alric, Benjamin
Gruber, Heike
Held, Christoph
author_sort Dégletagne, Cyril
title Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
title_short Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
title_full Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
title_fullStr Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
title_full_unstemmed Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica
title_sort presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve arctica islandica
publisher Nature Publishing Group UK
publishDate 2021
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8452683/
http://www.ncbi.nlm.nih.gov/pubmed/34545198
https://doi.org/10.1038/s42003-021-02593-1
genre Arctica islandica
Ocean quahog
genre_facet Arctica islandica
Ocean quahog
op_source Commun Biol
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8452683/
http://www.ncbi.nlm.nih.gov/pubmed/34545198
http://dx.doi.org/10.1038/s42003-021-02593-1
op_rights © The Author(s) 2021
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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
op_rightsnorm CC-BY
op_doi https://doi.org/10.1038/s42003-021-02593-1
container_title Communications Biology
container_volume 4
container_issue 1
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