Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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Curtis, Bruce A., Tanifuji, Goro, Maruyama, Shinichiro, Gile, Gillian H., Hopkins, Julia F., Eveleigh, Robert J. M., Nakayama, Takuro, Malik, Shehre Banoo, Onodera, Naoko T., Slamovits, Claudio H., Spencer, David F., Lane, Christopher E., Gray, Michael W., Archibald, John M., Burki, Fabien, Hirakawa, Yoshihisa, Reyes-Prieto, Adrian, Keeling, Patrick J., Fast, Naomi M., Green, Beverley R., Grisdale, Cameron J., Gruber, Ansgar, Kroth, Peter G., Irimia, Manuel, Arias, Maria C., Ball, Steven G., Kuo, Alan, Schmutz, Jeremy, Grimwood, Jane, Lindquist, Erika, Lucas, Susan, Salamov, Asaf, Grigoriev, Igor V., Rensing, Stefan A., Symeonidi, Aikaterini, Elias, Marek, Herman, Emily K., Klute, Mary J., Dacks, Joel B., Oborník, Miroslav, Kořený, Luděk, Durnford, Dion G., Neilson, Jonathan A. D., Armbrust, E. Virginia, Rocap, Gabrielle, Aves, Stephen J., Liu, Yuan, Beiko, Robert G., Coutinho, Pedro, Henrissat, Bernard, Hempel, Franziska, Maier, Uwe G., Zauner, Stefan, Häppner, Marc P., Ishida, Ken Ichiro, Shirato, Shu, Suzuki, Shigekatsu, Kim, Eunsoo, Richards, Thomas A., McRose, Darcy, Worden, Alexandra Z., Mock, Thomas ORCID: https://orcid.org/0000-0001-9604-0362, Poole, Anthony M., Pritham, Ellen J., Roy, Scott W., Schaack, Sarah, Bell, Callum, Bharti, Arvind K., Crow, John A., Kramer, Robin and McFadden, Geoffrey I. (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature, 492 (7427). pp. 59-65. ISSN 0028-0836

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Abstract

Cryptophyte and chlorarachniophyte algae are transitional forms in the widespread secondary endosymbiotic acquisition of photosynthesis by engulfment of eukaryotic algae. Unlike most secondary plastid-bearing algae, miniaturized versions of the endosymbiont nuclei (nucleomorphs) persist in cryptophytes and chlorarachniophytes. To determine why, and to address other fundamental questions about eukaryote–eukaryote endosymbiosis, we sequenced the nuclear genomes of the cryptophyte Guillardia theta and the chlorarachniophyte Bigelowiella natans. Both genomes have <21, 000 protein genes and are intron rich, and B. natans exhibits unprecedented alternative splicing for a single-celled organism. Phylogenomic analyses and subcellular targeting predictions reveal extensive genetic and biochemical mosaicism, with both host- and endosymbiont-derived genes servicing the mitochondrion, the host cell cytosol, the plastid and the remnant endosymbiont cytosol of both algae. Mitochondrion-to-nucleus gene transfer still occurs in both organisms but plastid-to-nucleus and nucleomorph-to-nucleus transfers do not, which explains why a small residue of essential genes remains locked in each nucleomorph.

Item Type: Article
Additional Information: Funding Information: Acknowledgements The work conducted by theUSDepartment of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. RNA-seq data used in the paper were generated by the National Center for Genome Resources as part of the Gordon and Betty Moore Foundation’s Marine Microbial Eukaryote Transcriptome Project. B.A.C. and J.F.H. were supported by a Special Research Opportunities Grant from the Natural Sciences and Engineering Research Council of Canada awarded to J.M.A. and M.W.G. J.M.A., P.J.K., M.W.G. and C.H.S. are members of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity. G.I.M. is an Australian Research Council Federation Fellow and a Howard Hughes International Scholar. We thank R. A. Andersen (Bigelow Laboratories) for assistance with single-cell isolations, C. X. Chan for a tree-sorting PERL script, H. Gutierrez for help with SM protein family annotation, and B. Read for permission to analyse the Emiliania huxleyi genome sequenced by the JGI.
Uncontrolled Keywords: general ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School: Faculty of Science > School of Environmental Sciences
UEA Research Groups: Faculty of Science > Research Groups > Centre for Ocean and Atmospheric Sciences
Faculty of Science > Research Groups > Environmental Biology
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Depositing User: LivePure Connector
Date Deposited: 08 Mar 2024 12:33
Last Modified: 08 Mar 2024 14:32
URI: https://ueaeprints.uea.ac.uk/id/eprint/94601
DOI: 10.1038/nature11681

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