Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid

ABSTRACT Perkinsela is an enigmatic early-branching kinetoplastid protist that lives as an obligate endosymbiont inside Paramoeba (Amoebozoa). We have sequenced the highly reduced mitochondrial genome of Perkinsela, which possesses only six protein-coding genes (cox1, cox2, cox3, cob, atp6, and rps1...

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Autores principales: Vojtěch David, Pavel Flegontov, Evgeny Gerasimov, Goro Tanifuji, Hassan Hashimi, Maria D. Logacheva, Shinichiro Maruyama, Naoko T. Onodera, Michael W. Gray, John M. Archibald, Julius Lukeš
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Publicado: American Society for Microbiology 2015
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spelling oai:doaj.org-article:cece96b2c0254a7580ba024afffa40042021-11-15T15:41:24ZGene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid10.1128/mBio.01498-152150-7511https://doaj.org/article/cece96b2c0254a7580ba024afffa40042015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01498-15https://doaj.org/toc/2150-7511ABSTRACT Perkinsela is an enigmatic early-branching kinetoplastid protist that lives as an obligate endosymbiont inside Paramoeba (Amoebozoa). We have sequenced the highly reduced mitochondrial genome of Perkinsela, which possesses only six protein-coding genes (cox1, cox2, cox3, cob, atp6, and rps12), despite the fact that the organelle itself contains more DNA than is present in either the host or endosymbiont nuclear genomes. An in silico analysis of two Perkinsela strains showed that mitochondrial RNA editing and processing machineries typical of kinetoplastid flagellates are generally conserved, and all mitochondrial transcripts undergo U-insertion/deletion editing. Canonical kinetoplastid mitochondrial ribosomes are also present. We have developed software tools for accurate and exhaustive mapping of transcriptome sequencing (RNA-seq) reads with extensive U-insertions/deletions, which allows detailed investigation of RNA editing via deep sequencing. With these methods, we show that up to 50% of reads for a given edited region contain errors of the editing system or, less likely, correspond to alternatively edited transcripts. IMPORTANCE Uridine insertion/deletion-type RNA editing, which occurs in the mitochondrion of kinetoplastid protists, has been well-studied in the model parasite genera Trypanosoma, Leishmania, and Crithidia. Perkinsela provides a unique opportunity to broaden our knowledge of RNA editing machinery from an evolutionary perspective, as it represents the earliest kinetoplastid branch and is an obligatory endosymbiont with extensive reductive trends. Interestingly, up to 50% of mitochondrial transcripts in Perkinsela contain errors. Our study was complemented by use of newly developed software designed for accurate mapping of extensively edited RNA-seq reads obtained by deep sequencing.Vojtěch DavidPavel FlegontovEvgeny GerasimovGoro TanifujiHassan HashimiMaria D. LogachevaShinichiro MaruyamaNaoko T. OnoderaMichael W. GrayJohn M. ArchibaldJulius LukešAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Vojtěch David
Pavel Flegontov
Evgeny Gerasimov
Goro Tanifuji
Hassan Hashimi
Maria D. Logacheva
Shinichiro Maruyama
Naoko T. Onodera
Michael W. Gray
John M. Archibald
Julius Lukeš
Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
description ABSTRACT Perkinsela is an enigmatic early-branching kinetoplastid protist that lives as an obligate endosymbiont inside Paramoeba (Amoebozoa). We have sequenced the highly reduced mitochondrial genome of Perkinsela, which possesses only six protein-coding genes (cox1, cox2, cox3, cob, atp6, and rps12), despite the fact that the organelle itself contains more DNA than is present in either the host or endosymbiont nuclear genomes. An in silico analysis of two Perkinsela strains showed that mitochondrial RNA editing and processing machineries typical of kinetoplastid flagellates are generally conserved, and all mitochondrial transcripts undergo U-insertion/deletion editing. Canonical kinetoplastid mitochondrial ribosomes are also present. We have developed software tools for accurate and exhaustive mapping of transcriptome sequencing (RNA-seq) reads with extensive U-insertions/deletions, which allows detailed investigation of RNA editing via deep sequencing. With these methods, we show that up to 50% of reads for a given edited region contain errors of the editing system or, less likely, correspond to alternatively edited transcripts. IMPORTANCE Uridine insertion/deletion-type RNA editing, which occurs in the mitochondrion of kinetoplastid protists, has been well-studied in the model parasite genera Trypanosoma, Leishmania, and Crithidia. Perkinsela provides a unique opportunity to broaden our knowledge of RNA editing machinery from an evolutionary perspective, as it represents the earliest kinetoplastid branch and is an obligatory endosymbiont with extensive reductive trends. Interestingly, up to 50% of mitochondrial transcripts in Perkinsela contain errors. Our study was complemented by use of newly developed software designed for accurate mapping of extensively edited RNA-seq reads obtained by deep sequencing.
format article
author Vojtěch David
Pavel Flegontov
Evgeny Gerasimov
Goro Tanifuji
Hassan Hashimi
Maria D. Logacheva
Shinichiro Maruyama
Naoko T. Onodera
Michael W. Gray
John M. Archibald
Julius Lukeš
author_facet Vojtěch David
Pavel Flegontov
Evgeny Gerasimov
Goro Tanifuji
Hassan Hashimi
Maria D. Logacheva
Shinichiro Maruyama
Naoko T. Onodera
Michael W. Gray
John M. Archibald
Julius Lukeš
author_sort Vojtěch David
title Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
title_short Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
title_full Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
title_fullStr Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
title_full_unstemmed Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic Kinetoplastid
title_sort gene loss and error-prone rna editing in the mitochondrion of <italic toggle="yes">perkinsela</italic>, an endosymbiotic kinetoplastid
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/cece96b2c0254a7580ba024afffa4004
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