TY - JOUR
T1 - Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis
AU - Sarai, Chihiro
AU - Tanifuji, Goro
AU - Nakayama, Takuro
AU - Kamikawa, Ryoma
AU - Takahashi, Kazuya
AU - Yazaki, Euki
AU - Matsuo, Eriko
AU - Miyashita, Hideaki
AU - Ishida, Ken ichiro
AU - Iwataki, Mitsunori
AU - Inagaki, Yuji
N1 - Funding Information:
ACKNOWLEDGMENTS. The authors thank Dr. Bruce A. Curtis (Dalhousie University, Canada) for proofreading an early draft of this manuscript. This work was supported in part by the Japan Society for the Promotion of Sciences Grants 23117006, 16H04826, 18KK0203, and 19H03280 (to Y.I.), 25304029 and 15H04533 (to M.I.), 17H03723 and 26840123 (to G.T.) 14J05929 (to C.S.), 17K15164 (to T.N.), and 19H03274 (to R.K.); Ministry of Education, Culture, Sports, Science and Technology of Japan Grant-in-Aid for Scientific Research on Innovative Areas 3308; a research grant from The Yanmar Environmental Sustainability Support Association (to R.K.); and the “Tree of Life” research project of the University of Tsukuba. Phylogenetic analyses of the 75-protein alignment were carried out under the “Interdisciplinary Computational Science Program” in the Center for Computational Sciences, University of Tsukuba.
Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.
PY - 2020/3/10
Y1 - 2020/3/10
N2 - 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.
AB - 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.
KW - Endosymbiotic gene transfer
KW - Nucleomorph
KW - Pedinophyceae
KW - Plastid
KW - Secondary endosymbiosis
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U2 - 10.1073/pnas.1911884117
DO - 10.1073/pnas.1911884117
M3 - Article
C2 - 32094181
AN - SCOPUS:85081657905
VL - 117
SP - 5364
EP - 5375
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 10
ER -