Pan genome of the phytoplankton Emiliania underpins its global distribution

Betsy A. Read, Jessica Kegel, Mary J. Klute, Alan Kuo, Stephane C. Lefebvre, Florian Maumus, Christoph Mayer, John Miller, Adam Monier, Asaf Salamov, Jeremy Young, Maria Aguilar, Jean Michel Claverie, Stephan Frickenhaus, Karina Gonzalez, Emily K. Herman, Yao Cheng Lin, Johnathan Napier, Hiroyuki Ogata, Analissa F. Sarno & 58 others Jeremy Shmutz, Declan Schroeder, Colomban De Vargas, Frederic Verret, Peter Von Dassow, Klaus Valentin, Yves Van De Peer, Glen Wheeler, Joel B. Dacks, Charles F. Delwiche, Sonya T. Dyhrman, Gernot Glöckner, Uwe John, Thomas Richards, Alexandra Z. Worden, Xiaoyu Zhang, Igor V. Grigoriev, Andrew E. Allen, Kay Bidle, Mark Borodovsky, Chris Bowler, Colin Brownlee, J. Mark Cock, Marek Elias, Vadim N. Gladyshev, Marco Groth, Chittibabu Guda, Ahmad Hadaegh, Maria Debora Iglesias-Rodriguez, Jerry Jenkins, Bethan M. Jones, Tracy Lawson, Florian Leese, Erika Lindquist, Alexei Lobanov, Alexandre Lomsadze, Shehre Banoo Malik, Mary E. Marsh, Luke MacKinder, Thomas Mock, Bernd Mueller-Roeber, António Pagarete, Micaela Parker, Ian Probert, Hadi Quesneville, Christine Raines, Stefan A. Rensing, Diego Mauricio Riaño-Pachón, Sophie Richier, Sebastian Rokitta, Yoshihiro Shiraiwa, Darren M. Soanes, Mark Van Der Giezen, Thomas M. Wahlund, Bryony Williams, Willie Wilson, Gordon Wolfe, Louie L. Wurch

Research output: Contribution to journalArticle

225 Citations (Scopus)

Abstract

Coccolithophores have influenced the global climate for over 200 million years. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO 2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO 2 production or uptake, sequestration and export to the deep ocean. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.

Original languageEnglish (US)
Pages (from-to)209-213
Number of pages5
JournalNature
Volume499
Issue number7457
DOIs
StatePublished - Jun 17 2013

Fingerprint

Haptophyta
Phytoplankton
Genome
Carbon Cycle
Calcium Carbonate
Carbon Monoxide
Oceans and Seas
Nucleic Acid Repetitive Sequences
Climate
Genes
Ecosystem
Carbon

ASJC Scopus subject areas

  • General

Cite this

Read, B. A., Kegel, J., Klute, M. J., Kuo, A., Lefebvre, S. C., Maumus, F., ... Wurch, L. L. (2013). Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature, 499(7457), 209-213. https://doi.org/10.1038/nature12221

Pan genome of the phytoplankton Emiliania underpins its global distribution. / Read, Betsy A.; Kegel, Jessica; Klute, Mary J.; Kuo, Alan; Lefebvre, Stephane C.; Maumus, Florian; Mayer, Christoph; Miller, John; Monier, Adam; Salamov, Asaf; Young, Jeremy; Aguilar, Maria; Claverie, Jean Michel; Frickenhaus, Stephan; Gonzalez, Karina; Herman, Emily K.; Lin, Yao Cheng; Napier, Johnathan; Ogata, Hiroyuki; Sarno, Analissa F.; Shmutz, Jeremy; Schroeder, Declan; De Vargas, Colomban; Verret, Frederic; Von Dassow, Peter; Valentin, Klaus; Van De Peer, Yves; Wheeler, Glen; Dacks, Joel B.; Delwiche, Charles F.; Dyhrman, Sonya T.; Glöckner, Gernot; John, Uwe; Richards, Thomas; Worden, Alexandra Z.; Zhang, Xiaoyu; Grigoriev, Igor V.; Allen, Andrew E.; Bidle, Kay; Borodovsky, Mark; Bowler, Chris; Brownlee, Colin; Mark Cock, J.; Elias, Marek; Gladyshev, Vadim N.; Groth, Marco; Guda, Chittibabu; Hadaegh, Ahmad; Iglesias-Rodriguez, Maria Debora; Jenkins, Jerry; Jones, Bethan M.; Lawson, Tracy; Leese, Florian; Lindquist, Erika; Lobanov, Alexei; Lomsadze, Alexandre; Malik, Shehre Banoo; Marsh, Mary E.; MacKinder, Luke; Mock, Thomas; Mueller-Roeber, Bernd; Pagarete, António; Parker, Micaela; Probert, Ian; Quesneville, Hadi; Raines, Christine; Rensing, Stefan A.; Riaño-Pachón, Diego Mauricio; Richier, Sophie; Rokitta, Sebastian; Shiraiwa, Yoshihiro; Soanes, Darren M.; Van Der Giezen, Mark; Wahlund, Thomas M.; Williams, Bryony; Wilson, Willie; Wolfe, Gordon; Wurch, Louie L.

In: Nature, Vol. 499, No. 7457, 17.06.2013, p. 209-213.

Research output: Contribution to journalArticle

Read, BA, Kegel, J, Klute, MJ, Kuo, A, Lefebvre, SC, Maumus, F, Mayer, C, Miller, J, Monier, A, Salamov, A, Young, J, Aguilar, M, Claverie, JM, Frickenhaus, S, Gonzalez, K, Herman, EK, Lin, YC, Napier, J, Ogata, H, Sarno, AF, Shmutz, J, Schroeder, D, De Vargas, C, Verret, F, Von Dassow, P, Valentin, K, Van De Peer, Y, Wheeler, G, Dacks, JB, Delwiche, CF, Dyhrman, ST, Glöckner, G, John, U, Richards, T, Worden, AZ, Zhang, X, Grigoriev, IV, Allen, AE, Bidle, K, Borodovsky, M, Bowler, C, Brownlee, C, Mark Cock, J, Elias, M, Gladyshev, VN, Groth, M, Guda, C, Hadaegh, A, Iglesias-Rodriguez, MD, Jenkins, J, Jones, BM, Lawson, T, Leese, F, Lindquist, E, Lobanov, A, Lomsadze, A, Malik, SB, Marsh, ME, MacKinder, L, Mock, T, Mueller-Roeber, B, Pagarete, A, Parker, M, Probert, I, Quesneville, H, Raines, C, Rensing, SA, Riaño-Pachón, DM, Richier, S, Rokitta, S, Shiraiwa, Y, Soanes, DM, Van Der Giezen, M, Wahlund, TM, Williams, B, Wilson, W, Wolfe, G & Wurch, LL 2013, 'Pan genome of the phytoplankton Emiliania underpins its global distribution', Nature, vol. 499, no. 7457, pp. 209-213. https://doi.org/10.1038/nature12221
Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F et al. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature. 2013 Jun 17;499(7457):209-213. https://doi.org/10.1038/nature12221
Read, Betsy A. ; Kegel, Jessica ; Klute, Mary J. ; Kuo, Alan ; Lefebvre, Stephane C. ; Maumus, Florian ; Mayer, Christoph ; Miller, John ; Monier, Adam ; Salamov, Asaf ; Young, Jeremy ; Aguilar, Maria ; Claverie, Jean Michel ; Frickenhaus, Stephan ; Gonzalez, Karina ; Herman, Emily K. ; Lin, Yao Cheng ; Napier, Johnathan ; Ogata, Hiroyuki ; Sarno, Analissa F. ; Shmutz, Jeremy ; Schroeder, Declan ; De Vargas, Colomban ; Verret, Frederic ; Von Dassow, Peter ; Valentin, Klaus ; Van De Peer, Yves ; Wheeler, Glen ; Dacks, Joel B. ; Delwiche, Charles F. ; Dyhrman, Sonya T. ; Glöckner, Gernot ; John, Uwe ; Richards, Thomas ; Worden, Alexandra Z. ; Zhang, Xiaoyu ; Grigoriev, Igor V. ; Allen, Andrew E. ; Bidle, Kay ; Borodovsky, Mark ; Bowler, Chris ; Brownlee, Colin ; Mark Cock, J. ; Elias, Marek ; Gladyshev, Vadim N. ; Groth, Marco ; Guda, Chittibabu ; Hadaegh, Ahmad ; Iglesias-Rodriguez, Maria Debora ; Jenkins, Jerry ; Jones, Bethan M. ; Lawson, Tracy ; Leese, Florian ; Lindquist, Erika ; Lobanov, Alexei ; Lomsadze, Alexandre ; Malik, Shehre Banoo ; Marsh, Mary E. ; MacKinder, Luke ; Mock, Thomas ; Mueller-Roeber, Bernd ; Pagarete, António ; Parker, Micaela ; Probert, Ian ; Quesneville, Hadi ; Raines, Christine ; Rensing, Stefan A. ; Riaño-Pachón, Diego Mauricio ; Richier, Sophie ; Rokitta, Sebastian ; Shiraiwa, Yoshihiro ; Soanes, Darren M. ; Van Der Giezen, Mark ; Wahlund, Thomas M. ; Williams, Bryony ; Wilson, Willie ; Wolfe, Gordon ; Wurch, Louie L. / Pan genome of the phytoplankton Emiliania underpins its global distribution. In: Nature. 2013 ; Vol. 499, No. 7457. pp. 209-213.
@article{716f60071d424525a3d88986cb44c1d6,
title = "Pan genome of the phytoplankton Emiliania underpins its global distribution",
abstract = "Coccolithophores have influenced the global climate for over 200 million years. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO 2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO 2 production or uptake, sequestration and export to the deep ocean. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.",
author = "Read, {Betsy A.} and Jessica Kegel and Klute, {Mary J.} and Alan Kuo and Lefebvre, {Stephane C.} and Florian Maumus and Christoph Mayer and John Miller and Adam Monier and Asaf Salamov and Jeremy Young and Maria Aguilar and Claverie, {Jean Michel} and Stephan Frickenhaus and Karina Gonzalez and Herman, {Emily K.} and Lin, {Yao Cheng} and Johnathan Napier and Hiroyuki Ogata and Sarno, {Analissa F.} and Jeremy Shmutz and Declan Schroeder and {De Vargas}, Colomban and Frederic Verret and {Von Dassow}, Peter and Klaus Valentin and {Van De Peer}, Yves and Glen Wheeler and Dacks, {Joel B.} and Delwiche, {Charles F.} and Dyhrman, {Sonya T.} and Gernot Gl{\"o}ckner and Uwe John and Thomas Richards and Worden, {Alexandra Z.} and Xiaoyu Zhang and Grigoriev, {Igor V.} and Allen, {Andrew E.} and Kay Bidle and Mark Borodovsky and Chris Bowler and Colin Brownlee and {Mark Cock}, J. and Marek Elias and Gladyshev, {Vadim N.} and Marco Groth and Chittibabu Guda and Ahmad Hadaegh and Iglesias-Rodriguez, {Maria Debora} and Jerry Jenkins and Jones, {Bethan M.} and Tracy Lawson and Florian Leese and Erika Lindquist and Alexei Lobanov and Alexandre Lomsadze and Malik, {Shehre Banoo} and Marsh, {Mary E.} and Luke MacKinder and Thomas Mock and Bernd Mueller-Roeber and Ant{\'o}nio Pagarete and Micaela Parker and Ian Probert and Hadi Quesneville and Christine Raines and Rensing, {Stefan A.} and Ria{\~n}o-Pach{\'o}n, {Diego Mauricio} and Sophie Richier and Sebastian Rokitta and Yoshihiro Shiraiwa and Soanes, {Darren M.} and {Van Der Giezen}, Mark and Wahlund, {Thomas M.} and Bryony Williams and Willie Wilson and Gordon Wolfe and Wurch, {Louie L.}",
year = "2013",
month = "6",
day = "17",
doi = "10.1038/nature12221",
language = "English (US)",
volume = "499",
pages = "209--213",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "7457",

}

TY - JOUR

T1 - Pan genome of the phytoplankton Emiliania underpins its global distribution

AU - Read, Betsy A.

AU - Kegel, Jessica

AU - Klute, Mary J.

AU - Kuo, Alan

AU - Lefebvre, Stephane C.

AU - Maumus, Florian

AU - Mayer, Christoph

AU - Miller, John

AU - Monier, Adam

AU - Salamov, Asaf

AU - Young, Jeremy

AU - Aguilar, Maria

AU - Claverie, Jean Michel

AU - Frickenhaus, Stephan

AU - Gonzalez, Karina

AU - Herman, Emily K.

AU - Lin, Yao Cheng

AU - Napier, Johnathan

AU - Ogata, Hiroyuki

AU - Sarno, Analissa F.

AU - Shmutz, Jeremy

AU - Schroeder, Declan

AU - De Vargas, Colomban

AU - Verret, Frederic

AU - Von Dassow, Peter

AU - Valentin, Klaus

AU - Van De Peer, Yves

AU - Wheeler, Glen

AU - Dacks, Joel B.

AU - Delwiche, Charles F.

AU - Dyhrman, Sonya T.

AU - Glöckner, Gernot

AU - John, Uwe

AU - Richards, Thomas

AU - Worden, Alexandra Z.

AU - Zhang, Xiaoyu

AU - Grigoriev, Igor V.

AU - Allen, Andrew E.

AU - Bidle, Kay

AU - Borodovsky, Mark

AU - Bowler, Chris

AU - Brownlee, Colin

AU - Mark Cock, J.

AU - Elias, Marek

AU - Gladyshev, Vadim N.

AU - Groth, Marco

AU - Guda, Chittibabu

AU - Hadaegh, Ahmad

AU - Iglesias-Rodriguez, Maria Debora

AU - Jenkins, Jerry

AU - Jones, Bethan M.

AU - Lawson, Tracy

AU - Leese, Florian

AU - Lindquist, Erika

AU - Lobanov, Alexei

AU - Lomsadze, Alexandre

AU - Malik, Shehre Banoo

AU - Marsh, Mary E.

AU - MacKinder, Luke

AU - Mock, Thomas

AU - Mueller-Roeber, Bernd

AU - Pagarete, António

AU - Parker, Micaela

AU - Probert, Ian

AU - Quesneville, Hadi

AU - Raines, Christine

AU - Rensing, Stefan A.

AU - Riaño-Pachón, Diego Mauricio

AU - Richier, Sophie

AU - Rokitta, Sebastian

AU - Shiraiwa, Yoshihiro

AU - Soanes, Darren M.

AU - Van Der Giezen, Mark

AU - Wahlund, Thomas M.

AU - Williams, Bryony

AU - Wilson, Willie

AU - Wolfe, Gordon

AU - Wurch, Louie L.

PY - 2013/6/17

Y1 - 2013/6/17

N2 - Coccolithophores have influenced the global climate for over 200 million years. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO 2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO 2 production or uptake, sequestration and export to the deep ocean. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.

AB - Coccolithophores have influenced the global climate for over 200 million years. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO 2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO 2 production or uptake, sequestration and export to the deep ocean. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions.

UR - http://www.scopus.com/inward/record.url?scp=84880511242&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84880511242&partnerID=8YFLogxK

U2 - 10.1038/nature12221

DO - 10.1038/nature12221

M3 - Article

VL - 499

SP - 209

EP - 213

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7457

ER -