Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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

doi:10.1038/nature11681

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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

Department of Life Science

Research output: Contribution to journal › Article › peer-review

312 Scopus citations

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.

Original language	English
Pages (from-to)	59-65
Number of pages	7
Journal	Nature
Volume	492
Issue number	7427
DOIs	https://doi.org/10.1038/nature11681
State	Published - 6 Dec 2012

Bibliographical note

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.

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Curtis, B. A., Tanifuji, G., Maruyama, S., Gile, G. H., Hopkins, J. F., Eveleigh, R. J. M., Nakayama, T., Malik, S. B., Onodera, N. T., Slamovits, C. H., Spencer, D. F., Lane, C. E., Gray, M. W., Archibald, J. M., Burki, F., Hirakawa, Y., Reyes-Prieto, A., Keeling, P. J., Fast, N. M., ... Mc Fadden, G. I. (2012). Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature, 492(7427), 59-65. https://doi.org/10.1038/nature11681

@article{684113216be14ae58c7fa673cf165357,

title = "Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs",

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.",

author = "Curtis, {Bruce A.} and Goro Tanifuji and Shinichiro Maruyama and Gile, {Gillian H.} and Hopkins, {Julia F.} and Eveleigh, {Robert J.M.} and Takuro Nakayama and Malik, {Shehre Banoo} and Onodera, {Naoko T.} and Slamovits, {Claudio H.} and Spencer, {David F.} and Lane, {Christopher E.} and Gray, {Michael W.} and Archibald, {John M.} and Fabien Burki and Yoshihisa Hirakawa and Adrian Reyes-Prieto and Keeling, {Patrick J.} and Fast, {Naomi M.} and Green, {Beverley R.} and Grisdale, {Cameron J.} and Ansgar Gruber and Kroth, {Peter G.} and Manuel Irimia and Arias, {Maria C.} and Ball, {Steven G.} and Alan Kuo and Jeremy Schmutz and Jane Grimwood and Erika Lindquist and Susan Lucas and Asaf Salamov and Grigoriev, {Igor V.} and Rensing, {Stefan A.} and Aikaterini Symeonidi and Marek Elias and Herman, {Emily K.} and Klute, {Mary J.} and Dacks, {Joel B.} and Miroslav Oborn{\'i}k and Lud{\v e}k Ko{\v r}en{\'y} and Durnford, {Dion G.} and Neilson, {Jonathan A.D.} and Armbrust, {E. Virginia} and Gabrielle Rocap and Aves, {Stephen J.} and Yuan Liu and Beiko, {Robert G.} and Pedro Coutinho and Bernard Henrissat and Franziska Hempel and Maier, {Uwe G.} and Stefan Zauner and H{\"a}ppner, {Marc P.} and Ishida, {Ken Ichiro} and Shu Shirato and Shigekatsu Suzuki and Eunsoo Kim and Richards, {Thomas A.} and {Mc Rose}, Darcy and Worden, {Alexandra Z.} and Thomas Mock and Poole, {Anthony M.} and Pritham, {Ellen J.} and Roy, {Scott W.} and Sarah Schaack and Callum Bell and Bharti, {Arvind K.} and Crow, {John A.} and Robin Kramer and {Mc Fadden}, {Geoffrey I.}",

note = "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{\textquoteright}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.",

year = "2012",

month = dec,

day = "6",

doi = "10.1038/nature11681",

language = "English",

volume = "492",

pages = "59--65",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7427",

}

Curtis, BA, Tanifuji, G, Maruyama, S, Gile, GH, Hopkins, JF, Eveleigh, RJM, Nakayama, T, Malik, SB, Onodera, NT, Slamovits, CH, Spencer, DF, Lane, CE, Gray, MW, Archibald, JM, Burki, F, Hirakawa, Y, Reyes-Prieto, A, Keeling, PJ, Fast, NM, Green, BR, Grisdale, CJ, Gruber, A, Kroth, PG, Irimia, M, Arias, MC, Ball, SG, Kuo, A, Schmutz, J, Grimwood, J, Lindquist, E, Lucas, S, Salamov, A, Grigoriev, IV, Rensing, SA, Symeonidi, A, Elias, M, Herman, EK, Klute, MJ, Dacks, JB, Oborník, M, Kořený, L, Durnford, DG, Neilson, JAD, Armbrust, EV, Rocap, G, Aves, SJ, Liu, Y, Beiko, RG, Coutinho, P, Henrissat, B, Hempel, F, Maier, UG, Zauner, S, Häppner, MP, Ishida, KI, Shirato, S, Suzuki, S, Kim, E, Richards, TA, Mc Rose, D, Worden, AZ, Mock, T, Poole, AM, Pritham, EJ, Roy, SW, Schaack, S, Bell, C, Bharti, AK, Crow, JA, Kramer, R & Mc Fadden, GI 2012, 'Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs', Nature, vol. 492, no. 7427, pp. 59-65. https://doi.org/10.1038/nature11681

TY - JOUR

T1 - Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

AU - Curtis, Bruce A.

AU - Tanifuji, Goro

AU - Maruyama, Shinichiro

AU - Gile, Gillian H.

AU - Hopkins, Julia F.

AU - Eveleigh, Robert J.M.

AU - Nakayama, Takuro

AU - Malik, Shehre Banoo

AU - Onodera, Naoko T.

AU - Slamovits, Claudio H.

AU - Spencer, David F.

AU - Lane, Christopher E.

AU - Gray, Michael W.

AU - Archibald, John M.

AU - Burki, Fabien

AU - Hirakawa, Yoshihisa

AU - Reyes-Prieto, Adrian

AU - Keeling, Patrick J.

AU - Fast, Naomi M.

AU - Green, Beverley R.

AU - Grisdale, Cameron J.

AU - Gruber, Ansgar

AU - Kroth, Peter G.

AU - Irimia, Manuel

AU - Arias, Maria C.

AU - Ball, Steven G.

AU - Kuo, Alan

AU - Schmutz, Jeremy

AU - Grimwood, Jane

AU - Lindquist, Erika

AU - Lucas, Susan

AU - Salamov, Asaf

AU - Grigoriev, Igor V.

AU - Rensing, Stefan A.

AU - Symeonidi, Aikaterini

AU - Elias, Marek

AU - Herman, Emily K.

AU - Klute, Mary J.

AU - Dacks, Joel B.

AU - Oborník, Miroslav

AU - Kořený, Luděk

AU - Durnford, Dion G.

AU - Neilson, Jonathan A.D.

AU - Armbrust, E. Virginia

AU - Rocap, Gabrielle

AU - Aves, Stephen J.

AU - Liu, Yuan

AU - Beiko, Robert G.

AU - Coutinho, Pedro

AU - Henrissat, Bernard

AU - Hempel, Franziska

AU - Maier, Uwe G.

AU - Zauner, Stefan

AU - Häppner, Marc P.

AU - Ishida, Ken Ichiro

AU - Shirato, Shu

AU - Suzuki, Shigekatsu

AU - Kim, Eunsoo

AU - Richards, Thomas A.

AU - Mc Rose, Darcy

AU - Worden, Alexandra Z.

AU - Mock, Thomas

AU - Poole, Anthony M.

AU - Pritham, Ellen J.

AU - Roy, Scott W.

AU - Schaack, Sarah

AU - Bell, Callum

AU - Bharti, Arvind K.

AU - Crow, John A.

AU - Kramer, Robin

AU - Mc Fadden, Geoffrey I.

N1 - 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.

PY - 2012/12/6

Y1 - 2012/12/6

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84870564943&partnerID=8YFLogxK

U2 - 10.1038/nature11681

DO - 10.1038/nature11681

M3 - Article

C2 - 23201678

AN - SCOPUS:84870564943

SN - 0028-0836

VL - 492

SP - 59

EP - 65

JO - Nature

JF - Nature

IS - 7427

ER -

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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