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Maturyoshka: a maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes

View ORCID ProfileKacper Maciszewski, View ORCID ProfileNadja Dabbagh, Angelika Preisfeld, View ORCID ProfileAnna Karnkowska
doi: https://doi.org/10.1101/2021.09.24.461685
Kacper Maciszewski
aInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Żwirki i Wigury 101, 02-089, Warsaw, Poland
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  • ORCID record for Kacper Maciszewski
Nadja Dabbagh
bZoology and Didactics of Biology, Faculty of Mathematics and Natural Sciences, Bergische University Wuppertal, Gaussstraße 20, Wuppertal, 42119, Germany
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Angelika Preisfeld
bZoology and Didactics of Biology, Faculty of Mathematics and Natural Sciences, Bergische University Wuppertal, Gaussstraße 20, Wuppertal, 42119, Germany
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Anna Karnkowska
aInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Żwirki i Wigury 101, 02-089, Warsaw, Poland
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  • For correspondence: a.karnkowska@uw.edu.pl
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Abstract

Organellar genomes often carry group II introns, which occasionally encode proteins called maturases that are important for splicing. The number of introns varies substantially among various organellar genomes, and bursts of introns have been observed in multiple eukaryotic lineages, including euglenophytes, with more than 100 introns in their plastid genomes. To examine the evolutionary diversity and history of maturases, an essential gene family among euglenophytes, we searched for their homologs in newly sequenced and published plastid genomes representing all major euglenophytes’ lineages. We found that maturase content in plastid genomes has a patchy distribution, with a maximum of eight of them present in Eutreptiella eupharyngea. The most basal lineages of euglenophytes, Eutreptiales, share the highest number of maturases, but the lowest number of introns. We also identified a peculiar convoluted structure of a gene located in an intron, in a gene within an intron, within yet another gene, present in some Eutreptiales. Further investigation of functional domains of identified maturases shown that most of them lost at least one of the functional domains, which implies that the patchy maturase distribution is due to frequent inactivation and eventual loss over time. Finally, we identified the diversified evolutionary origin of analysed maturases, which were acquired along with the green algal plastid or horizontally transferred. These findings indicate that euglenophytes’ plastid maturases have experienced a surprisingly dynamic history due to gains from diversified donors, their retention, and loss.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    GIIM
    group II intron maturase
    HNHE
    HNH endonuclease
    IEP
    intron-encoded protein
    ORF
    open reading frame
    ptDNA
    plastid DNA, plastid genome
    RVT
    reverse transcriptase/maturase
    SSU rDNA
    small subunit of the ribosomal DNA
  • Copyright 
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    Maturyoshka: a maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes
    Kacper Maciszewski, Nadja Dabbagh, Angelika Preisfeld, Anna Karnkowska
    bioRxiv 2021.09.24.461685; doi: https://doi.org/10.1101/2021.09.24.461685
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    Maturyoshka: a maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes
    Kacper Maciszewski, Nadja Dabbagh, Angelika Preisfeld, Anna Karnkowska
    bioRxiv 2021.09.24.461685; doi: https://doi.org/10.1101/2021.09.24.461685

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