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Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis

Chihiro Sarai, Goro Tanifuji, Takuro Nakayama, Ryoma Kamikawa, Kazuya Takahashi, Hideaki Miyashita, Ken-ichiro Ishida, Mitsunori Iwataki, View ORCID ProfileYuji Inagaki
doi: https://doi.org/10.1101/702274
Chihiro Sarai
Graduate School of Science and Engineering and Science, Yamagata University, Yamagata 990-8560, Japan
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Goro Tanifuji
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, JapanDepartment of Zoology, National Museum of Nature and Science, Tsukuba, 305-0005, Japan
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  • For correspondence: yuji@ccs.tsukuba.ac.jp iwataki@anesc.u-tokyo.ac.jp gorot@kahaku.go.jp
Takuro Nakayama
Center for Computational Sciences, University of Tsukuba, Tsukuba 305-8577, JapanDepartment of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Sendai, 980-8578, Japan
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Ryoma Kamikawa
Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Kazuya Takahashi
Graduate School of Science and Engineering and Science, Yamagata University, Yamagata 990-8560, JapanAsian Natural Environmental Science Center, The University of Tokyo, Tokyo 113-8657, Japan
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Hideaki Miyashita
Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Ken-ichiro Ishida
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, Japan
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Mitsunori Iwataki
Graduate School of Science and Engineering and Science, Yamagata University, Yamagata 990-8560, JapanAsian Natural Environmental Science Center, The University of Tokyo, Tokyo 113-8657, Japan
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  • For correspondence: yuji@ccs.tsukuba.ac.jp iwataki@anesc.u-tokyo.ac.jp gorot@kahaku.go.jp
Yuji Inagaki
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, JapanCenter for Computational Sciences, University of Tsukuba, Tsukuba 305-8577, Japan
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  • ORCID record for Yuji Inagaki
  • For correspondence: yuji@ccs.tsukuba.ac.jp iwataki@anesc.u-tokyo.ac.jp gorot@kahaku.go.jp
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Abstract

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 integrating an endosymbiont alga into be a host-governed plastid (organellogenesis). Nevertheless, past studies suggested 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 difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which from-endosymbiont-to-host DNA transfer is on-going and of 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 the evidence for the presence of DNA in the two nucleomorphs and 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 MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. Combined, we conclude that the host-endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as new models for elucidating organellogenesis.

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Posted July 14, 2019.
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Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis
Chihiro Sarai, Goro Tanifuji, Takuro Nakayama, Ryoma Kamikawa, Kazuya Takahashi, Hideaki Miyashita, Ken-ichiro Ishida, Mitsunori Iwataki, Yuji Inagaki
bioRxiv 702274; doi: https://doi.org/10.1101/702274
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Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis
Chihiro Sarai, Goro Tanifuji, Takuro Nakayama, Ryoma Kamikawa, Kazuya Takahashi, Hideaki Miyashita, Ken-ichiro Ishida, Mitsunori Iwataki, Yuji Inagaki
bioRxiv 702274; doi: https://doi.org/10.1101/702274

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