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Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

The Raphidophyceae is an ecologically important eukaryotic lineage of primary producers and predators that inhabit marine and freshwater environments worldwide. These organisms are of great evolutionary interest because their plastids are the product of eukaryote-eukaryote endosymbiosis. To obtain d...

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Autores principales: Kim, Jong Im, Jo, Bok Yeon, Park, Myung Gil, Yoo, Yeong Du, Shin, Woongghi, Archibald, John M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9235467/
https://www.ncbi.nlm.nih.gov/pubmed/35769291
http://dx.doi.org/10.3389/fpls.2022.896138
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author Kim, Jong Im
Jo, Bok Yeon
Park, Myung Gil
Yoo, Yeong Du
Shin, Woongghi
Archibald, John M.
author_facet Kim, Jong Im
Jo, Bok Yeon
Park, Myung Gil
Yoo, Yeong Du
Shin, Woongghi
Archibald, John M.
author_sort Kim, Jong Im
collection PubMed
description The Raphidophyceae is an ecologically important eukaryotic lineage of primary producers and predators that inhabit marine and freshwater environments worldwide. These organisms are of great evolutionary interest because their plastids are the product of eukaryote-eukaryote endosymbiosis. To obtain deeper insight into the evolutionary history of raphidophycean plastids, we sequenced and analyzed the plastid genomes of three freshwater and three marine species. Our comparison of these genomes, together with the previously reported plastid genome of Heterosigma akashiwo, revealed unexpected variability in genome structure. Unlike the genomes of other analyzed species, the plastid genome of Gonyostomum semen was found to contain only a single rRNA operon, presumably due to the loss of genes from the inverted repeat (IR) region found in most plastid genomes. In contrast, the marine species Fibrocapsa japonica contains the largest IR region and overall plastid genome for any raphidophyte examined thus far, mainly due to the presence of four large gene-poor regions and foreign DNA. Two plastid genes, tyrC in F. japonica and He. akashiwo and serC in F. japonica, appear to have arisen via lateral gene transfer (LGT) from diatoms, and several raphidophyte open reading frames are demonstrably homologous to sequences in diatom plasmids and plastid genomes. A group II intron in the F. japonica psbB gene also appears to be derived by LGT. Our results provide important insights into the evolutionary history of raphidophyte plastid genomes via LGT from the plastids and plasmid DNAs of diatoms.
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spelling pubmed-92354672022-06-28 Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes Kim, Jong Im Jo, Bok Yeon Park, Myung Gil Yoo, Yeong Du Shin, Woongghi Archibald, John M. Front Plant Sci Plant Science The Raphidophyceae is an ecologically important eukaryotic lineage of primary producers and predators that inhabit marine and freshwater environments worldwide. These organisms are of great evolutionary interest because their plastids are the product of eukaryote-eukaryote endosymbiosis. To obtain deeper insight into the evolutionary history of raphidophycean plastids, we sequenced and analyzed the plastid genomes of three freshwater and three marine species. Our comparison of these genomes, together with the previously reported plastid genome of Heterosigma akashiwo, revealed unexpected variability in genome structure. Unlike the genomes of other analyzed species, the plastid genome of Gonyostomum semen was found to contain only a single rRNA operon, presumably due to the loss of genes from the inverted repeat (IR) region found in most plastid genomes. In contrast, the marine species Fibrocapsa japonica contains the largest IR region and overall plastid genome for any raphidophyte examined thus far, mainly due to the presence of four large gene-poor regions and foreign DNA. Two plastid genes, tyrC in F. japonica and He. akashiwo and serC in F. japonica, appear to have arisen via lateral gene transfer (LGT) from diatoms, and several raphidophyte open reading frames are demonstrably homologous to sequences in diatom plasmids and plastid genomes. A group II intron in the F. japonica psbB gene also appears to be derived by LGT. Our results provide important insights into the evolutionary history of raphidophyte plastid genomes via LGT from the plastids and plasmid DNAs of diatoms. Frontiers Media S.A. 2022-05-26 /pmc/articles/PMC9235467/ /pubmed/35769291 http://dx.doi.org/10.3389/fpls.2022.896138 Text en Copyright © 2022 Kim, Jo, Park, Yoo, Shin and Archibald. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Kim, Jong Im
Jo, Bok Yeon
Park, Myung Gil
Yoo, Yeong Du
Shin, Woongghi
Archibald, John M.
Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title_full Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title_fullStr Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title_full_unstemmed Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title_short Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes
title_sort evolutionary dynamics and lateral gene transfer in raphidophyceae plastid genomes
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9235467/
https://www.ncbi.nlm.nih.gov/pubmed/35769291
http://dx.doi.org/10.3389/fpls.2022.896138
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