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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2015-12-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01498-15 |
| _version_ | 1818754353849171968 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T05:21:55Z |
| format | Article |
| id | doaj.art-cece96b2c0254a7580ba024afffa4004 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T05:21:55Z |
| publishDate | 2015-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-cece96b2c0254a7580ba024afffa40042022-12-21T21:19:38ZengAmerican Society for MicrobiologymBio2150-75112015-12-016610.1128/mBio.01498-15Gene Loss and Error-Prone RNA Editing in the Mitochondrion of <italic toggle="yes">Perkinsela</italic>, an Endosymbiotic KinetoplastidVojtěch David0Pavel Flegontov1Evgeny Gerasimov2Goro Tanifuji3Hassan Hashimi4Maria D. Logacheva5Shinichiro Maruyama6Naoko T. Onodera7Michael W. Gray8John M. Archibald9Julius Lukeš10Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech RepublicInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech RepublicFaculty of Biology, Lomonosov Moscow State University, Moscow, RussiaDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, CanadaInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech RepublicFaculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, RussiaDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, CanadaDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, CanadaDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, CanadaDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, CanadaInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech RepublicABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.01498-15 |
| spellingShingle | 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 mBio |
| title | 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_short | 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 |
| url | https://journals.asm.org/doi/10.1128/mBio.01498-15 |
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