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Dinoflagellates with Relic Endosymbiont Nuclei As Models for Elucidating Organellogenesis

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Dinoflagellates with Relic Endosymbiont Nuclei As Models for Elucidating Organellogenesis Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis Chihiro Saraia,1, Goro Tanifujib,c,1,2, Takuro Nakayamad,e,1, Ryoma Kamikawaf,1, Kazuya Takahashia,g, Euki Yazakih, Eriko Matsuoi, Hideaki Miyashitaf, Ken-ichiro Ishidab, Mitsunori Iwatakia,g,2, and Yuji Inagakid,i,2 aGraduate School of Science and Engineering, Yamagata University, 990-8560 Yamagata, Japan; bFaculty of Life and Environmental Sciences, University of Tsukuba, 305-8572 Tsukuba, Japan; cDepartment of Zoology, National Museum of Nature and Science, 305-0005 Tsukuba, Japan; dCenter for Computational Sciences, University of Tsukuba, 305-8577 Tsukuba, Japan; eGraduate School of Life Sciences, Tohoku University, 980-8578 Sendai, Japan; fGraduate School of Human and Environmental Studies, Kyoto University, 606-8501 Kyoto, Japan; gAsian Natural Environmental Science Center, The University of Tokyo, 113-8657 Tokyo, Japan; hDepartment of Biochemistry and Molecular Biology, Graduate School and Faculty of Medicine, The University of Tokyo, 113-0033 Tokyo, Japan; and iGraduate School of Life and Environmental Sciences, University of Tsukuba, 305-8572 Tsukuba, Japan Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved January 29, 2020 (received for review July 15, 2019) Nucleomorphs are relic endosymbiont nuclei so far found only in The evolutionary process of integrating an endosymbiont into two algal groups, cryptophytes and chlorarachniophytes, which the host cell (organellogenesis) has yet to be fully understood. have been studied to model the evolutionary process of integrat- Nevertheless, genomic data from diverse eukaryotic lineages ing an endosymbiont alga into a host-governed plastid (organello- indicated that endosymbiont genomes should have lost a massive genesis). However, past studies suggest that DNA transfer from number of genes that were dispensable for intracellular/endo- the endosymbiont to host nuclei had already ceased in both symbiotic lifestyles (1–5). It is most likely that the reduction of cryptophytes and chlorarachniophytes, implying that the organ- endosymbiont genomes and integration of the endosymbiont into ellogenesis at the genetic level has been completed in the two the host progressed simultaneously during organellogenesis (1– systems. Moreover, we have yet to pinpoint the closest free-living 4). The reductive process that occurred in endosymbiont ge- relative of the endosymbiotic alga engulfed by the ancestral nomes seemingly has a tight correlation with genome G + C chlorarachniophyte or cryptophyte, making it difficult to infer content (GC%), as reduced endosymbiont genomes are com- how organellogenesis altered the endosymbiont genome. To monly poor in G and C (6–9). To interlock the host and endo- counter the above issues, we need novel nucleomorph-bearing symbiont metabolically and genetically, we regard, transfer of EVOLUTION algae, in which endosymbiont-to-host DNA transfer is on-going endosymbiont genes to the host nuclear genome (endosymbiotic and for which endosymbiont/plastid origins can be inferred at a ’ fine taxonomic scale. Here, we report two previously undescribed gene transfer, EGT), coupled with the host s invention of ma- dinoflagellates, strains MGD and TGD, with green algal endosym- chineries that enable them to express the transferred genes and bionts enclosing plastids as well as relic nuclei (nucleomorphs). We target the gene products to the original compartment, as critical provide evidence for the presence of DNA in the two nucleo- morphs and the transfer of endosymbiont genes to the host (di- Significance noflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both We report here two previously undescribed dinoflagellates the MGD and TGD systems. Phylogenetic analyses successfully re- that can be models for elucidating the genome evolution as- solved the origins of the endosymbionts at the genus level. With sociated with transforming an endosymbiotic alga into a the combined evidence, we conclude that the host–endosymbiont plastid (organellogenesis). The two dinoflagellate strains pos- integration in MGD/TGD is less advanced than that in crypto- sess green algal endosymbionts enclosing the plastids and relic phytes/chrorarachniophytes, and propose the two dinoflagellates nuclei (nucleomorphs). Our analyses indicated that DNA as models for elucidating organellogenesis. transfer from the nucleomorph to the host nuclear genome is in progress in both dinoflagellates, even though their endo- secondary endosymbiosis | nucleomorph | endosymbiotic gene transfer | symbiotic algae have been transformed into organelles (plas- plastid | Pedinophyceae tids). Moreover, the origins of the two endosymbionts were resolved at the genus level. These two features found in the he transformation of a free-living photosynthetic organism two dinoflagellates are absent from well-studied nucleomorph- Tinto a plastid through endosymbiosis has occurred multiple bearing algal lineages, namely cryptophytes and chlorar- times in eukaryotic evolution. The first plastid was most likely achniophytes. Consequently, the two dinoflagellates assist us in established through “primary endosymbiosis” between a cyano- understanding endosymbiosis-driven eukaryotic genome evolu- bacterium and the common ancestor of red, glaucophyte, and tion at a finer scale. green algae (plus descendants of green algae, i.e., land plants) – Author contributions: G.T., M.I., and Y.I. designed research; C.S., G.T., T.N., R.K., K.T., H.M., (1 4). The plastids in the three lineages described above are the and K.-i.I. performed research; C.S., K.T., K.-i.I., and M.I. isolated and cultivated the two direct descendants of the cyanobacterial endosymbiont, and strains of dinoflagellates used in this study; G.T., T.N., R.K., E.Y., E.M., and Y.I. analyzed designated as “primary plastids.” After major eukaryotic lineages data; and C.S., G.T., T.N., R.K., M.I., and Y.I. wrote the paper. diverged, some heterotrophs turned into phototrophs by ac- The authors declare no competing interest. quiring “secondary plastids” through algal endosymbionts bear- This article is a PNAS Direct Submission. ing primary plastids (secondary endosymbioses). Secondary Published under the PNAS license. endosymbioses most likely occurred multiple times in eukaryotic Data deposition: The transcriptome data from the dinoflagellate strains MGD and TGD evolution, as the host lineages bearing secondary plastids (so- are available from the DNA Data Bank Japan (BioProject PRJDB8237). called complex algae) are distantly related to one another (1– 1C.S., G.T., T.N., and R.K. contributed equally to this work. 4). In addition, the origins of secondary plastids vary among 2To whom correspondence may be addressed. Email: [email protected], iwataki@ complex algae; some possess red alga-derived plastids, while anesc.u-tokyo.ac.jp, or [email protected]. others possess green alga-derived plastids, strongly arguing that This article contains supporting information online at https://www.pnas.org/lookup/suppl/ the two types of secondary plastids were established through doi:10.1073/pnas.1911884117/-/DCSupplemental. separate (at least two) endosymbiotic events (1–4). www.pnas.org/cgi/doi/10.1073/pnas.1911884117 PNAS Latest Articles | 1of12 Downloaded by guest on October 1, 2021 (1–4, 10). Nevertheless, the precise process that enables organ- molecular evidence for the diatom endosymbionts being modified ellogenesis still remains unclear. extensively during the endosymbiosis (54, 60–64). No intracellular structures of the endosymbiotic algae were Here, we report two undescribed dinoflagellates, strains MGD left except plastids in most of the complex algae (euglenids, and TGD, with green alga-derived plastids containing Chls a+b. chromerids, haptophytes, ochrophytes, and dinoflagellates). Only The two dinoflagellates are distinct from each other in terms of cryptophytes and chlorarachniophytes are known to retain nucle- their cell morphologies, and no clear affinity between the two omorphs, the relic nuclei of their algal endosymbionts (1, 8, 9, 11, hosts was recovered by molecular phylogenetic analyses. In both 12). As the two complex algae bearing nucleomorphs possess the MGD and TGD, conspicuous nucleus-like structures with DNA morphological characteristics that have been lost from others, were identified in the periplastidal compartments (PPCs) that they were thought to provide clues to understand the detailed correspond to the endosymbiont cytoplasm. We successfully process of organellogenesis (1, 8, 9). In this regard, the genomic obtained evidence for the green algal endosymbionts being data of both nuclei and nucleomorphs, as well as transcriptomic genetically integrated into the dinoflagellate host cells. Both and proteomic data, have been accumulated for cryptophytes and green algal endosymbionts showed clear phylogenetic affinities to chlorarachniophytes (13–22), and genetic transformation was Pedinophyceae, a particular group of green algae. Taken together, established for a chlorarachniophyte species (23). It has been these observations lead us to conclude that MGD and TGD are determined that a red alga and an ulvophyte green alga are nucleomorph-bearing organisms harboring Chls a+b-containing the sources of cryptophyte and chlorarachniophyte plastids, re- plastids derived from endosymbiotic Pedinophyceae green algae. spectively (18, 24–28), but an even recent multigene phylogenetic
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