Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ. Evry, Université Paris-Saclay, 91057, Evry, France.
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, 11794, USA.
BMC Biol. 2021 Jan 6;19(1):1. doi: 10.1186/s12915-020-00927-9.
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.
甲藻是一种水生原生生物，在全球海洋中广泛存在。有些甲藻会引发有毒藻类大量繁殖，而另一些则与其他原生生物和动物形成共生关系，如珊瑚中的互惠共生体或感染其他原生生物的寄生虫。甲藻拥有非典型的大型基因组（约 3 到 250 Gb），其基因组织和基因表达模式与密切相关的顶复门寄生虫非常不同。在这里，我们对两种早期分化且共生的寄生甲藻 Amoebophrya 菌株进行了测序和分析，以揭示这种非典型基因组特征的出现、甲藻的进化以及宿主特化的机制。
我们使用 Illumina 配对末端短读测序和 Oxford Nanopore Technology（ONT）MinION 长读测序方法相结合，对两种 Amoebophrya 菌株（A25 和 A120）进行了测序、组装和注释，获得了高质量的基因组。我们发现，少量转座元件、短的内含子和基因间区以及有限数量的基因家族共同导致了 Amoebophrya 基因组的紧凑性，这一特征可能与寄生有关。虽然 Amoebophrya 的大多数蛋白（A25 的 63.7%和 A120 的 59.3%）没有功能注释，但我们发现了许多与 Dinophyceae 共享的同源基因。我们的分析表明，尽管种间蛋白序列相似性较低，但两个基因组之间存在强烈的单向聚类基因编码趋势和高水平的基因同线性保守性，这表明蛋白质进化迅速。最引人注目的是，我们鉴定出了大量非典型内含子，包括重复内含子，这些内含子表现出广泛的剪接基序多样性，在真核生物中从未观察到。这些内含子元件似乎具有在各自基因组中传播的能力，类似于转座元件。最后，我们证实了 Amoebophrya spp. 中细胞器的减少，即质体的丧失、线粒体基因组和功能的潜在丧失。
这些结果扩展了在基础甲藻中发现的非典型基因组特征的范围，并提出了关于物种形成和进化机制的问题，同时也为在这个特定的单细胞谱系中选择寄生提供了依据。
