Graduate School of Science and Engineering, Yamagata University, 990-8560 Yamagata, Japan.
Faculty of Life and Environmental Sciences, University of Tsukuba, 305-8572 Tsukuba, Japan;
Proc Natl Acad Sci U S A. 2020 Mar 10;117(10):5364-5375. doi: 10.1073/pnas.1911884117. Epub 2020 Feb 24.
Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host-endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.
类核体是迄今为止仅在两个藻类群cryptophytes 和 chlorarachniophytes 中发现的共生体核的遗迹，这两个藻类群被用来模拟将共生藻类整合到宿主控制的质体（细胞器发生）的进化过程。然而，过去的研究表明，cryptophytes 和 chlorarachniophytes 中的共生体 DNA 向宿主核的转移已经停止，这意味着这两个系统在遗传水平上的细胞器发生已经完成。此外，我们还没有确定被祖先chlorarachniophyte 或 cryptophyte 吞噬的共生藻类的最接近的自由生活的近亲，因此很难推断细胞器发生如何改变了共生体基因组。为了解决上述问题，我们需要新型的带有类核体的藻类，其中共生体向宿主的 DNA 转移仍在进行，并且可以在精细的分类学尺度上推断内共生体/质体的起源。在这里，我们报告了两种以前未描述的甲藻，MGD 和 TGD 菌株，它们含有绿色藻类共生体，并且含有质体和遗迹核（类核体）。我们提供了这两个类核体中存在 DNA 以及共生体基因向宿主（甲藻）基因组转移的证据。此外，在 MGD 和 TGD 系统中都发现了宿主和共生体核之间的 DNA 转移正在进行。系统发育分析成功地解决了共生体在属水平上的起源问题。有了综合证据，我们得出结论，MGD/TGD 中的宿主-共生体整合不如 cryptophytes/chlorarachniophytes 先进，并提出这两种甲藻是阐明细胞器发生的模型。
