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A new lineage of non-photosynthetic green algae with extreme organellar genomes

Tomáš Pánek, Dovilė Barcytė, Sebastian C. Treitli, Kristína Záhonová, Martin Sokol, Tereza Ševčíková, Eliška Zadrobílková, Karin Jaške, Naoji Yubuki, Ivan Čepička, Marek Eliáš
doi: https://doi.org/10.1101/2021.11.17.468966
Tomáš Pánek
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
2Department of Zoology, Faculty of Science, Charles University, 128 43 Prague, Czech Republic
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Dovilė Barcytė
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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Sebastian C. Treitli
3Department of Parasitology, Faculty of Science, Charles University, BIOCEV, 252 42 Vestec, Czech Republic
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Kristína Záhonová
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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Martin Sokol
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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Tereza Ševčíková
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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Eliška Zadrobílková
2Department of Zoology, Faculty of Science, Charles University, 128 43 Prague, Czech Republic
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Karin Jaške
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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Naoji Yubuki
2Department of Zoology, Faculty of Science, Charles University, 128 43 Prague, Czech Republic
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Ivan Čepička
2Department of Zoology, Faculty of Science, Charles University, 128 43 Prague, Czech Republic
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Marek Eliáš
1Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00 Ostrava, Czech Republic
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  • For correspondence: marek.elias@osu.cz
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Abstract

Background The plastid genomes of the green algal order Chlamydomonadales tend to expand their non-coding regions, but this phenomenon is poorly understood. Here we shed new light on organellar genome evolution in Chlamydomonadales by studying a previously unknown non-photosynthetic lineage. We established cultures of two new Polytoma-like flagellates, defined their basic characteristics and phylogenetic position, and obtained complete organellar genome sequences and a transcriptome assembly for one of them.

Results We discovered a novel deeply diverged chlamydomonadalean lineage that has no close photosynthetic relatives and represents an independent case of photosynthesis loss. To accommodate these organisms, we establish a new genus, Leontynka, with two species L. pallida and L. elongata distinguished by both morphological and molecular characteristics. Notable features of the colourless plastid of L. pallida deduced from the plastid genome (plastome) sequence and transcriptome assembly include the retention of ATP synthase, thylakoid-associated proteins, carotenoid biosynthesis pathway, and plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the L. pallida plastome with its ∼362 kbp is by far the largest among non-photosynthetic eukaryotes investigated to date. Instead of a high gene content, its size reflects extreme proliferation of sequence repeats. These are present also in coding sequences, with one repeat type found in exons of 11 out of 34 protein-coding genes and up to 36 copies per gene, affecting thus the encoded proteins. The mitochondrial genome of L. pallida is likewise exceptionally large, with its >104 kbp surpassed only by the mitogenome of Haematococcus lacustris among all members of Chlamydomonadales studied so far. It is also bloated with repeats, yet completely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both organellar genomes have accumulated related repeats. Furthermore, the L. pallida mitogenome exhibits an extremely high GC content in both coding and non-coding regions and, strikingly, a high number of predicted G-quadruplexes.

Conclusions With the unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and becomes an interesting model for studying organellar genome evolution.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 19, 2021.
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A new lineage of non-photosynthetic green algae with extreme organellar genomes
Tomáš Pánek, Dovilė Barcytė, Sebastian C. Treitli, Kristína Záhonová, Martin Sokol, Tereza Ševčíková, Eliška Zadrobílková, Karin Jaške, Naoji Yubuki, Ivan Čepička, Marek Eliáš
bioRxiv 2021.11.17.468966; doi: https://doi.org/10.1101/2021.11.17.468966
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A new lineage of non-photosynthetic green algae with extreme organellar genomes
Tomáš Pánek, Dovilė Barcytė, Sebastian C. Treitli, Kristína Záhonová, Martin Sokol, Tereza Ševčíková, Eliška Zadrobílková, Karin Jaške, Naoji Yubuki, Ivan Čepička, Marek Eliáš
bioRxiv 2021.11.17.468966; doi: https://doi.org/10.1101/2021.11.17.468966

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