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

[Display omitted] •We obtained four new complete plastid genomes of marine photosynthetic euglenids.•Plastid-based phylogeny indicates both Eutreptiella and order Eutreptiales to be paraphyletic.•Plastid genomes of Eutreptiales possess unique group II intron maturase genes.•A majority of euglenid plastid-encoded maturases is functionally deficient.•Plastid-encoded maturases have diverse origins in euglenids, as some were acquired by HGT. 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 euglenophyte 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 show 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.