Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch

Ophirinina is a recently described suborder of jakobid protists (Excavata) with only one described species to date, Ophirina amphinema. Despite the acquisition and analysis of massive transcriptomic and mitogenomic sequence data from O. amphinema, its phylogenetic position among excavates remained i...

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Autores: Galindo, Luis Javier, Prokina, Kristina, Torruella, Guifré, López García, Purificación, Moreira, David
Tipo de recurso: artículo
Fecha de publicación:2023
País:España
Institución:Universitat Politècnica de Catalunya (UPC)
Repositorio:UPCommons. Portal del coneixement obert de la UPC
Idioma:inglés
OAI Identifier:oai:upcommons.upc.edu:2117/388134
Acceso en línea:https://hdl.handle.net/2117/388134
https://dx.doi.org/10.1093/gbe/evad058
Access Level:acceso abierto
Palabra clave:Eukaryotic cell genetics
Phylogeny
Excavata
Jakovida
Ophirinina
Mitochondrial genome
Phylogenomics
Genòmica
Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica
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spelling Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid BranchGalindo, Luis JavierProkina, KristinaTorruella, GuifréLópez García, PurificaciónMoreira, DavidEukaryotic cell geneticsPhylogenyExcavataJakovidaOphirininaMitochondrial genomePhylogenomicsGenòmicaÀrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::BioinformàticaOphirinina is a recently described suborder of jakobid protists (Excavata) with only one described species to date, Ophirina amphinema. Despite the acquisition and analysis of massive transcriptomic and mitogenomic sequence data from O. amphinema, its phylogenetic position among excavates remained inconclusive, branching as sister group either to all Jakobida or to all Discoba. From a morphological perspective, it has not only several typical jakobid features but also unusual traits for this group, including the morphology of mitochondrial cristae (sac-shaped to flattened-curved cristae) and the presence of two flagellar vanes. In this study, we have isolated, morphologically characterized, and sequenced genome and transcriptome data of two new Ophirinina species: Ophirina chinija sp. nov. and Agogonia voluta gen. et sp. nov. Ophirina chinija differs from O. amphinema in having rounded cell ends, subapically emerging flagella and a posterior cell protrusion. The much more distantly related A. voluta has several unique ultrastructural characteristics, including sac-shaped mitochondrial cristae and a complex “B” fiber. Phylogenomic analyses with a large conserved-marker dataset supported the monophyly of Ophirina and Agogonia within the Ophirinina and, more importantly, resolved the conflicting position of ophirinids as the sister clade to all other jakobids. The characterization of the mitochondrial genomes showed that Agogonia differs from all known gene-rich jakobid mitogenomes by the presence of two group II introns and their corresponding maturase protein genes. A phylogenetic analysis of the diversity of known maturases confirmed that the Agogonia proteins are highly divergent from each other and define distant families among the prokaryotic and eukaryotic maturases. This opens the intriguing possibility that, compared to other jakobids, Ophirinina may have retained additional mitochondrial elements that may help to understand the early diversification of eukaryotes and the evolution of mitochondria.We thank Dr. Sergey A. Karpov (Zoological Institute RAS) and Dr. Denis V. Tikhonenkov (IBIW RAS) for their helpful discussions on the ultrastructural observations, and Dr. Hwan Su Yoon (Sungkyunkwan University) for the mitochondrial marker alignments. This work was supported by the European Research Council (ERC) Advanced Grants “Protistworld” and “Plast-Evol” (322669 and 787904, respectively) and the Horizon 2020 research and innovation program under the Marie Skłodowska-Curie ITN project SINGEK H2020-MSCA-ITN-2015-675752 (http://www.singek.eu/). G.T. was supported by the 2019 BP 00208 Beatriu de Pinos-3 Postdoctoral Program (BP3; 801370).Peer ReviewedOxford University Press20232023-01-0120232023-05-31journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/2117/388134https://dx.doi.org/10.1093/gbe/evad058reponame:UPCommons. Portal del coneixement obert de la UPCinstname:Universitat Politècnica de Catalunya (UPC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial 4.0 Internationalhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:upcommons.upc.edu:2117/3881342026-05-27T15:37:01Z
dc.title.none.fl_str_mv Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
title Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
spellingShingle Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
Galindo, Luis Javier
Eukaryotic cell genetics
Phylogeny
Excavata
Jakovida
Ophirinina
Mitochondrial genome
Phylogenomics
Genòmica
Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica
title_short Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
title_full Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
title_fullStr Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
title_full_unstemmed Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
title_sort Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch
dc.creator.none.fl_str_mv Galindo, Luis Javier
Prokina, Kristina
Torruella, Guifré
López García, Purificación
Moreira, David
author Galindo, Luis Javier
author_facet Galindo, Luis Javier
Prokina, Kristina
Torruella, Guifré
López García, Purificación
Moreira, David
author_role author
author2 Prokina, Kristina
Torruella, Guifré
López García, Purificación
Moreira, David
author2_role author
author
author
author
dc.subject.none.fl_str_mv Eukaryotic cell genetics
Phylogeny
Excavata
Jakovida
Ophirinina
Mitochondrial genome
Phylogenomics
Genòmica
Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica
topic Eukaryotic cell genetics
Phylogeny
Excavata
Jakovida
Ophirinina
Mitochondrial genome
Phylogenomics
Genòmica
Àrees temàtiques de la UPC::Informàtica::Aplicacions de la informàtica::Bioinformàtica
description Ophirinina is a recently described suborder of jakobid protists (Excavata) with only one described species to date, Ophirina amphinema. Despite the acquisition and analysis of massive transcriptomic and mitogenomic sequence data from O. amphinema, its phylogenetic position among excavates remained inconclusive, branching as sister group either to all Jakobida or to all Discoba. From a morphological perspective, it has not only several typical jakobid features but also unusual traits for this group, including the morphology of mitochondrial cristae (sac-shaped to flattened-curved cristae) and the presence of two flagellar vanes. In this study, we have isolated, morphologically characterized, and sequenced genome and transcriptome data of two new Ophirinina species: Ophirina chinija sp. nov. and Agogonia voluta gen. et sp. nov. Ophirina chinija differs from O. amphinema in having rounded cell ends, subapically emerging flagella and a posterior cell protrusion. The much more distantly related A. voluta has several unique ultrastructural characteristics, including sac-shaped mitochondrial cristae and a complex “B” fiber. Phylogenomic analyses with a large conserved-marker dataset supported the monophyly of Ophirina and Agogonia within the Ophirinina and, more importantly, resolved the conflicting position of ophirinids as the sister clade to all other jakobids. The characterization of the mitochondrial genomes showed that Agogonia differs from all known gene-rich jakobid mitogenomes by the presence of two group II introns and their corresponding maturase protein genes. A phylogenetic analysis of the diversity of known maturases confirmed that the Agogonia proteins are highly divergent from each other and define distant families among the prokaryotic and eukaryotic maturases. This opens the intriguing possibility that, compared to other jakobids, Ophirinina may have retained additional mitochondrial elements that may help to understand the early diversification of eukaryotes and the evolution of mitochondria.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023-01-01
2023
2023-05-31
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/2117/388134
https://dx.doi.org/10.1093/gbe/evad058
url https://hdl.handle.net/2117/388134
https://dx.doi.org/10.1093/gbe/evad058
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial 4.0 International
http://creativecommons.org/licenses/by-nc/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial 4.0 International
http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:UPCommons. Portal del coneixement obert de la UPC
instname:Universitat Politècnica de Catalunya (UPC)
instname_str Universitat Politècnica de Catalunya (UPC)
reponame_str UPCommons. Portal del coneixement obert de la UPC
collection UPCommons. Portal del coneixement obert de la UPC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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