Dinoflagellates are aquatic protists particularly widespread in the oceans worldwide. Some are responsible for toxic blooms while others live in symbiotic relationships, either as mutualistic symbionts in corals or as parasites infecting other protists and animals. Dinoflagellates harbor atypically large genomes (~ 3 to 250 Gb), with gene organization and gene expression patterns very different from closely related apicomplexan parasites. Here we sequenced and analyzed the genomes of two early-diverging and co-occurring parasitic dinoflagellate Amoebophrya strains, to shed light on the emergence of such atypical genomic features, dinoflagellate evolution, and host specialization. We sequenced, assembled, and annotated high-quality genomes for two Amoebophrya strains (A25 and A120), using a combination of Illumina paired-end short-read and Oxford Nanopore Technology (ONT) MinION long-read sequencing approaches. We found a small number of transposable elements, along with short introns and intergenic regions, and a limited number of gene families, together contribute to the compactness of the Amoebophrya genomes, a feature potentially linked with parasitism. While the majority of Amoebophrya proteins (63.7% of A25 and 59.3% of A120) had no functional assignment, we found many orthologs shared with Dinophyceae. Our analyses revealed a strong tendency for genes encoded by unidirectional clusters and high levels of synteny conservation between the two genomes despite low interspecific protein sequence similarity, suggesting rapid protein evolution. Most strikingly, we identified a large portion of non-canonical introns, including repeated introns, displaying a broad variability of associated splicing motifs never observed among eukaryotes. Those introner elements appear to have the capacity to spread over their respective genomes in a manner similar to transposable elements. Finally, we confirmed the reduction of organelles observed in Amoebophrya spp., i.e., loss of the plastid, potential loss of a mitochondrial genome and functions. These results expand the range of atypical genome features found in basal dinoflagellates and raise questions regarding speciation and the evolutionary mechanisms at play while parastitism was selected for in this particular unicellular lineage.

中文翻译：

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海洋需氧寄生虫甲藻变形虫中的快速蛋白质进化、细胞器减少和侵入性内含子元件

甲藻是水生原生生物，在世界各地的海洋中特别广泛。有些是有毒藻华的罪魁祸首，而另一些则以共生关系生活，要么作为珊瑚中的互利共生体，要么作为感染其他原生生物和动物的寄生虫。甲藻拥有非典型的大基因组（约 3 至 250 Gb），其基因组织和基因表达模式与密切相关的顶端复门寄生虫非常不同。在这里，我们对两种早期分化和共存的寄生甲藻变形虫菌株的基因组进行了测序和分析，以阐明这种非典型基因组特征、甲藻进化和宿主特化的出现。我们结合使用 Illumina 双端短读长和牛津纳米孔技术 (ONT) MinION 长读长测序方法，对两种变形虫菌株（A25 和 A120）的高质量基因组进行了测序、组装和注释。我们发现少量的转座元件、短的内含子和基因间区域以及有限数量的基因家族共同促成了变形虫基因组的紧凑性，这一特征可能与寄生有关。虽然大多数变形虫蛋白（A25 的 63.7% 和 A120 的 59.3%）没有功能分配，但我们发现许多与甲藻共有的直系同源物。我们的分析揭示了单向簇编码的基因的强烈趋势以及两个基因组之间高水平的同线性保守性，尽管种间蛋白质序列相似性较低，这表明蛋白质进化迅速。最引人注目的是，我们鉴定了很大一部分非规范内含子，包括重复内含子，显示出在真核生物中从未观察到的相关剪接基序的广泛变异性。这些内含子元件似乎能够以类似于转座元件的方式在各自的基因组中传播。最后，我们证实了在变形虫属中观察到的细胞器的减少，即质体的损失，线粒体基因组和功能的潜在损失。这些结果扩大了基底甲藻中发现的非典型基因组特征的范围，并提出了有关物种形成和进化机制的问题，同时在这种特殊的单细胞谱系中选择了寄生性。