Department of Biology and Ecology, Faculty of Science, University of Ostrava, 701 00, Ostrava, Czech Republic.
Department of Zoology, Faculty of Science, Charles University, 128 43, Prague, Czech Republic.
BMC Biol. 2022 Mar 17;20(1):66. doi: 10.1186/s12915-022-01263-w.
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.
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 the new genus Leontynka, with two species (L. pallida and L. elongata) distinguishable through both their 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, the carotenoid biosynthesis pathway, and a plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the ~362 kbp plastome of L. pallida is by far the largest among the non-photosynthetic eukaryotes investigated to date due to an extreme proliferation of sequence repeats. These repeats are also present in coding sequences, with one repeat type found in the exons of 11 out of 34 protein-coding genes, with up to 36 copies per gene, thus affecting 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 hitherto studied. It is also bloated with repeats, though entirely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both the 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.
With its unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and is an interesting model for studying organellar genome evolution.
绿藻门的衣藻目质体基因组往往会扩大其非编码区，但这一现象尚未得到充分理解。在这里，我们通过研究一个以前未知的非光合谱系，为衣藻目质体基因组的演化提供了新的见解。我们建立了两个新的 Polytoma 样鞭毛藻的培养物，确定了它们的基本特征和系统发育地位，并获得了其中一个的完整质体基因组序列和转录组组装。
我们发现了一个新的、深度分化的衣藻目谱系，它没有密切的光合近亲，代表了光合作用丧失的一个独立案例。为了容纳这些生物，我们建立了新的属 Leontynka，其中两个物种（L. pallida 和 L. elongata）可以通过它们的形态和分子特征来区分。从质体基因组（质体基因组）序列和转录组组装中推断出 L. pallida 无色质体的显著特征包括保留了 ATP 合酶、类囊体相关蛋白、类胡萝卜素生物合成途径和基于质醌的电子传递链，后两个模块与 Leontynka 中的眼点有明显的功能联系。最引人注目的是，L. pallida 的~362 kbp 质体基因组是迄今为止研究的非光合真核生物中最大的，因为序列重复的极度增殖。这些重复也存在于编码序列中，在 34 个蛋白质编码基因中的 11 个基因的外显子中发现了一种重复类型，每个基因多达 36 个拷贝，从而影响了编码的蛋白质。L. pallida 的线粒体基因组同样异常庞大，其>104 kbp 仅被迄今为止研究过的 Chlamydomonadales 成员中的 Haematococcus lacustris 的线粒体基因组超过。它也因重复而膨胀，尽管与 L. pallida 质体中的重复完全不同，这与 H. lacustris 的情况形成对比，在 H. lacustris 中，两个细胞器基因组都积累了相关的重复。此外，L. pallida 线粒体基因组在编码和非编码区域都具有极高的 GC 含量，并且令人惊讶的是，预测的 G-四联体数量非常多。
Leontynka 具有前所未有的质体和线粒体基因组特征组合，推动了细胞器基因组多样性的前沿，是研究细胞器基因组演化的有趣模型。
