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Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes

Mitochondrial genomes of apicomplexans, dinoflagellates, and chrompodellids that collectively make up the Myzozoa, encode only three proteins (Cytochrome b [COB], Cytochrome c oxidase subunit 1 [COX1], Cytochrome c oxidase subunit 3 [COX3]), contain fragmented ribosomal RNAs, and display extensive r...

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Autores principales: Gornik, Sebastian G, Flores, Victor, Reinhardt, Franziska, Erber, Lieselotte, Salas-Leiva, Dayana E, Douvropoulou, Olga, Lassadi, Imen, Einarsson, Elin, Mörl, Mario, Git, Anna, Stadler, Peter F, Pain, Arnab, Waller, Ross F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9550989/
https://www.ncbi.nlm.nih.gov/pubmed/36108082
http://dx.doi.org/10.1093/molbev/msac191
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author Gornik, Sebastian G
Flores, Victor
Reinhardt, Franziska
Erber, Lieselotte
Salas-Leiva, Dayana E
Douvropoulou, Olga
Lassadi, Imen
Einarsson, Elin
Mörl, Mario
Git, Anna
Stadler, Peter F
Pain, Arnab
Waller, Ross F
author_facet Gornik, Sebastian G
Flores, Victor
Reinhardt, Franziska
Erber, Lieselotte
Salas-Leiva, Dayana E
Douvropoulou, Olga
Lassadi, Imen
Einarsson, Elin
Mörl, Mario
Git, Anna
Stadler, Peter F
Pain, Arnab
Waller, Ross F
author_sort Gornik, Sebastian G
collection PubMed
description Mitochondrial genomes of apicomplexans, dinoflagellates, and chrompodellids that collectively make up the Myzozoa, encode only three proteins (Cytochrome b [COB], Cytochrome c oxidase subunit 1 [COX1], Cytochrome c oxidase subunit 3 [COX3]), contain fragmented ribosomal RNAs, and display extensive recombination, RNA trans-splicing, and RNA-editing. The early-diverging Perkinsozoa is the final major myzozoan lineage whose mitochondrial genomes remained poorly characterized. Previous reports of Perkinsus genes indicated independent acquisition of non-canonical features, namely the occurrence of multiple frameshifts. To determine both ancestral myzozoan and novel perkinsozoan mitochondrial genome features, we sequenced and assembled mitochondrial genomes of four Perkinsus species. These data show a simple ancestral genome with the common reduced coding capacity but disposition for rearrangement. We identified 75 frameshifts across the four species that occur as distinct types and that are highly conserved in gene location. A decoding mechanism apparently employs unused codons at the frameshift sites that advance translation either +1 or +2 frames to the next used codon. The locations of frameshifts are seemingly positioned to regulate protein folding of the nascent protein as it emerges from the ribosome. The cox3 gene is distinct in containing only one frameshift and showing strong selection against residues that are otherwise frequently encoded at the frameshift positions in cox1 and cob. All genes lack cysteine codons implying a reduction to 19 amino acids in these genomes. Furthermore, mitochondrion-encoded rRNA fragment complements are incomplete in Perkinsus spp. but some are found in the nuclear DNA suggesting import into the organelle. Perkinsus demonstrates further remarkable trajectories of organelle genome evolution including pervasive integration of frameshift translation into genome expression.
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spelling pubmed-95509892022-10-11 Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes Gornik, Sebastian G Flores, Victor Reinhardt, Franziska Erber, Lieselotte Salas-Leiva, Dayana E Douvropoulou, Olga Lassadi, Imen Einarsson, Elin Mörl, Mario Git, Anna Stadler, Peter F Pain, Arnab Waller, Ross F Mol Biol Evol Discoveries Mitochondrial genomes of apicomplexans, dinoflagellates, and chrompodellids that collectively make up the Myzozoa, encode only three proteins (Cytochrome b [COB], Cytochrome c oxidase subunit 1 [COX1], Cytochrome c oxidase subunit 3 [COX3]), contain fragmented ribosomal RNAs, and display extensive recombination, RNA trans-splicing, and RNA-editing. The early-diverging Perkinsozoa is the final major myzozoan lineage whose mitochondrial genomes remained poorly characterized. Previous reports of Perkinsus genes indicated independent acquisition of non-canonical features, namely the occurrence of multiple frameshifts. To determine both ancestral myzozoan and novel perkinsozoan mitochondrial genome features, we sequenced and assembled mitochondrial genomes of four Perkinsus species. These data show a simple ancestral genome with the common reduced coding capacity but disposition for rearrangement. We identified 75 frameshifts across the four species that occur as distinct types and that are highly conserved in gene location. A decoding mechanism apparently employs unused codons at the frameshift sites that advance translation either +1 or +2 frames to the next used codon. The locations of frameshifts are seemingly positioned to regulate protein folding of the nascent protein as it emerges from the ribosome. The cox3 gene is distinct in containing only one frameshift and showing strong selection against residues that are otherwise frequently encoded at the frameshift positions in cox1 and cob. All genes lack cysteine codons implying a reduction to 19 amino acids in these genomes. Furthermore, mitochondrion-encoded rRNA fragment complements are incomplete in Perkinsus spp. but some are found in the nuclear DNA suggesting import into the organelle. Perkinsus demonstrates further remarkable trajectories of organelle genome evolution including pervasive integration of frameshift translation into genome expression. Oxford University Press 2022-09-15 /pmc/articles/PMC9550989/ /pubmed/36108082 http://dx.doi.org/10.1093/molbev/msac191 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in anymedium, provided the originalwork is properly cited.
spellingShingle Discoveries
Gornik, Sebastian G
Flores, Victor
Reinhardt, Franziska
Erber, Lieselotte
Salas-Leiva, Dayana E
Douvropoulou, Olga
Lassadi, Imen
Einarsson, Elin
Mörl, Mario
Git, Anna
Stadler, Peter F
Pain, Arnab
Waller, Ross F
Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title_full Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title_fullStr Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title_full_unstemmed Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title_short Mitochondrial Genomes in Perkinsus Decode Conserved Frameshifts in All Genes
title_sort mitochondrial genomes in perkinsus decode conserved frameshifts in all genes
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9550989/
https://www.ncbi.nlm.nih.gov/pubmed/36108082
http://dx.doi.org/10.1093/molbev/msac191
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