Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

Bruce A. Curtis, Goro Tanifuji, Fabien Burki, Gillian Gile, Manuel Irimia, Shinichiro Maruyama, Maria C. Arias, Steven G. Ball, Gillian H. Gile, Yoshihisa Hirakawa, Julia F. Hopkins, Alan Kuo, Stefan A. Rensing, Jeremy Schmutz, Aikaterini Symeonidi, Marek Elias, Robert J M Eveleigh, Emily K. Herman, Mary J. Klute, Takuro Nakayama & 53 others Miroslav Oborník, Adrian Reyes-Prieto, E. Virginia Armbrust, Stephen J. Aves, Robert G. Beiko, Pedro Coutinho, Joel B. Dacks, Dion G. Durnford, Naomi M. Fast, Beverley R. Green, Cameron J. Grisdale, Franziska Hempel, Bernard Henrissat, Marc P. Höppner, Ken Ichiro Ishida, Eunsoo Kim, Luděk Kořený, Peter G. Kroth, Yuan Liu, Shehre Banoo Malik, Uwe G. Maier, Darcy McRose, Thomas Mock, Jonathan A D Neilson, Naoko T. Onodera, Anthony M. Poole, Ellen J. Pritham, Thomas A. Richards, Gabrielle Rocap, Scott W. Roy, Chihiro Sarai, Sarah Schaack, Shu Shirato, Claudio H. Slamovits, David F. Spencer, Shigekatsu Suzuki, Alexandra Z. Worden, Stefan Zauner, Kerrie Barry, Callum Bell, Arvind K. Bharti, John A. Crow, Jane Grimwood, Robin Kramer, Erika Lindquist, Susan Lucas, Asaf Salamov, Geoffrey I. McFadden, Christopher E. Lane, Patrick J. Keeling, Michael W. Gray, Igor V. Grigoriev, John M. Archibald

Research output: Contribution to journalArticle

228 Citations (Scopus)

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 >21,000protein 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.

Original languageEnglish (US)
Pages (from-to)59-65
Number of pages7
JournalNature
Volume491
Issue number7427
DOIs
StatePublished - Dec 6 2012
Externally publishedYes

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Plastids
Mosaicism
Genome
Eukaryota
Cytosol
Mitochondria
Genes
Symbiosis
Essential Genes
Alternative Splicing
Photosynthesis
Introns
Molecular Biology

ASJC Scopus subject areas

  • General

Cite this

Curtis, B. A., Tanifuji, G., Burki, F., Gile, G., Irimia, M., Maruyama, S., ... Archibald, J. M. (2012). Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature, 491(7427), 59-65. https://doi.org/10.1038/nature11681

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

In: Nature, Vol. 491, No. 7427, 06.12.2012, p. 59-65.

Research output: Contribution to journalArticle

Curtis, BA, Tanifuji, G, Burki, F, Gile, G, Irimia, M, Maruyama, S, Arias, MC, Ball, SG, Gile, GH, Hirakawa, Y, Hopkins, JF, Kuo, A, Rensing, SA, Schmutz, J, Symeonidi, A, Elias, M, Eveleigh, RJM, Herman, EK, Klute, MJ, Nakayama, T, Oborník, M, Reyes-Prieto, A, Virginia Armbrust, E, Aves, SJ, Beiko, RG, Coutinho, P, Dacks, JB, Durnford, DG, Fast, NM, Green, BR, Grisdale, CJ, Hempel, F, Henrissat, B, Höppner, MP, Ishida, KI, Kim, E, Kořený, L, Kroth, PG, Liu, Y, Malik, SB, Maier, UG, McRose, D, Mock, T, Neilson, JAD, Onodera, NT, Poole, AM, Pritham, EJ, Richards, TA, Rocap, G, Roy, SW, Sarai, C, Schaack, S, Shirato, S, Slamovits, CH, Spencer, DF, Suzuki, S, Worden, AZ, Zauner, S, Barry, K, Bell, C, Bharti, AK, Crow, JA, Grimwood, J, Kramer, R, Lindquist, E, Lucas, S, Salamov, A, McFadden, GI, Lane, CE, Keeling, PJ, Gray, MW, Grigoriev, IV & Archibald, JM 2012, 'Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs', Nature, vol. 491, no. 7427, pp. 59-65. https://doi.org/10.1038/nature11681
Curtis BA, Tanifuji G, Burki F, Gile G, Irimia M, Maruyama S et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature. 2012 Dec 6;491(7427):59-65. https://doi.org/10.1038/nature11681
Curtis, Bruce A. ; Tanifuji, Goro ; Burki, Fabien ; Gile, Gillian ; Irimia, Manuel ; Maruyama, Shinichiro ; Arias, Maria C. ; Ball, Steven G. ; Gile, Gillian H. ; Hirakawa, Yoshihisa ; Hopkins, Julia F. ; Kuo, Alan ; Rensing, Stefan A. ; Schmutz, Jeremy ; Symeonidi, Aikaterini ; Elias, Marek ; Eveleigh, Robert J M ; Herman, Emily K. ; Klute, Mary J. ; Nakayama, Takuro ; Oborník, Miroslav ; Reyes-Prieto, Adrian ; Virginia Armbrust, E. ; Aves, Stephen J. ; Beiko, Robert G. ; Coutinho, Pedro ; Dacks, Joel B. ; Durnford, Dion G. ; Fast, Naomi M. ; Green, Beverley R. ; Grisdale, Cameron J. ; Hempel, Franziska ; Henrissat, Bernard ; Höppner, Marc P. ; Ishida, Ken Ichiro ; Kim, Eunsoo ; Kořený, Luděk ; Kroth, Peter G. ; Liu, Yuan ; Malik, Shehre Banoo ; Maier, Uwe G. ; McRose, Darcy ; Mock, Thomas ; Neilson, Jonathan A D ; Onodera, Naoko T. ; Poole, Anthony M. ; Pritham, Ellen J. ; Richards, Thomas A. ; Rocap, Gabrielle ; Roy, Scott W. ; Sarai, Chihiro ; Schaack, Sarah ; Shirato, Shu ; Slamovits, Claudio H. ; Spencer, David F. ; Suzuki, Shigekatsu ; Worden, Alexandra Z. ; Zauner, Stefan ; Barry, Kerrie ; Bell, Callum ; Bharti, Arvind K. ; Crow, John A. ; Grimwood, Jane ; Kramer, Robin ; Lindquist, Erika ; Lucas, Susan ; Salamov, Asaf ; McFadden, Geoffrey I. ; Lane, Christopher E. ; Keeling, Patrick J. ; Gray, Michael W. ; Grigoriev, Igor V. ; Archibald, John M. / Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. In: Nature. 2012 ; Vol. 491, No. 7427. pp. 59-65.
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AU - Curtis, Bruce A.

AU - Tanifuji, Goro

AU - Burki, Fabien

AU - Gile, Gillian

AU - Irimia, Manuel

AU - Maruyama, Shinichiro

AU - Arias, Maria C.

AU - Ball, Steven G.

AU - Gile, Gillian H.

AU - Hirakawa, Yoshihisa

AU - Hopkins, Julia F.

AU - Kuo, Alan

AU - Rensing, Stefan A.

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AU - Symeonidi, Aikaterini

AU - Elias, Marek

AU - Eveleigh, Robert J M

AU - Herman, Emily K.

AU - Klute, Mary J.

AU - Nakayama, Takuro

AU - Oborník, Miroslav

AU - Reyes-Prieto, Adrian

AU - Virginia Armbrust, E.

AU - Aves, Stephen J.

AU - Beiko, Robert G.

AU - Coutinho, Pedro

AU - Dacks, Joel B.

AU - Durnford, Dion G.

AU - Fast, Naomi M.

AU - Green, Beverley R.

AU - Grisdale, Cameron J.

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AU - Kim, Eunsoo

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AU - Sarai, Chihiro

AU - Schaack, Sarah

AU - Shirato, Shu

AU - Slamovits, Claudio H.

AU - Spencer, David F.

AU - Suzuki, Shigekatsu

AU - Worden, Alexandra Z.

AU - Zauner, Stefan

AU - Barry, Kerrie

AU - Bell, Callum

AU - Bharti, Arvind K.

AU - Crow, John A.

AU - Grimwood, Jane

AU - Kramer, Robin

AU - Lindquist, Erika

AU - Lucas, Susan

AU - Salamov, Asaf

AU - McFadden, Geoffrey I.

AU - Lane, Christopher E.

AU - Keeling, Patrick J.

AU - Gray, Michael W.

AU - Grigoriev, Igor V.

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