Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans

Yoann Seeleuthner; Samuel Mondy; Vincent Lombard; Quentin Carradec; Eric Pelletier; Marc Wessner; Jade Leconte; Jean François Mangot; Julie Poulain; Karine Labadie; Ramiro Logares; Shinichi Sunagawa; Véronique De Berardinis; Marcel Salanoubat; Céline Dimier; Stefanie Kandels-Lewis; Marc Picheral; Sarah Searson; Silvia G. Acinas; Emmanuel Boss; Michael Follows; Gabriel Gorsky; Nigel Grimsley; Lee Karp-Boss; Uros Krzic; Fabrice Not; Hiroyuki Ogata; Jeroen Raes; Emmanuel G. Reynaud; Christian Sardet; Sabrina Speich; Lars Stemmann; Didier Velayoudon; Jean Weissenbach; Stephane Pesant; Nicole Poulton; Ramunas Stepanauskas; Peer Bork; Chris Bowler; Pascal Hingamp; Matthew B. Sullivan; Daniele Iudicone; Ramon Massana; Jean Marc Aury; Bernard Henrissat; Eric Karsenti; Olivier Jaillon; Mike Sieracki; Colomban De Vargas; Patrick Wincker

doi:10.1038/s41467-017-02235-3

Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans

Yoann Seeleuthner, Samuel Mondy, Vincent Lombard, Quentin Carradec, Eric Pelletier, Marc Wessner, Jade Leconte, Jean François Mangot, Julie Poulain, Karine Labadie, Ramiro Logares, Shinichi Sunagawa, Véronique De Berardinis, Marcel Salanoubat, Céline Dimier, Stefanie Kandels-Lewis, Marc Picheral, Sarah Searson, Silvia G. Acinas, Emmanuel BossMichael Follows, Gabriel Gorsky, Nigel Grimsley, Lee Karp-Boss, Uros Krzic, Fabrice Not, Hiroyuki Ogata, Jeroen Raes, Emmanuel G. Reynaud, Christian Sardet, Sabrina Speich, Lars Stemmann, Didier Velayoudon, Jean Weissenbach, Stephane Pesant, Nicole Poulton, Ramunas Stepanauskas, Peer Bork, Chris Bowler, Pascal Hingamp, Matthew B. Sullivan, Daniele Iudicone, Ramon Massana, Jean Marc Aury, Bernard Henrissat, Eric Karsenti, Olivier Jaillon, Mike Sieracki, Colomban De Vargas, Patrick Wincker

Ecology and Evolutionary Biology

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

51 Scopus citations

Abstract

Single-celled eukaryotes (protists) are critical players in global biogeochemical cycling of nutrients and energy in the oceans. While their roles as primary producers and grazers are well appreciated, other aspects of their life histories remain obscure due to challenges in culturing and sequencing their natural diversity. Here, we exploit single-cell genomics and metagenomics data from the circumglobal Tara Oceans expedition to analyze the genome content and apparent oceanic distribution of seven prevalent lineages of uncultured heterotrophic stramenopiles. Based on the available data, each sequenced genome or genotype appears to have a specific oceanic distribution, principally correlated with water temperature and depth. The genome content provides hypotheses for specialization in terms of cell motility, food spectra, and trophic stages, including the potential impact on their lifestyles of horizontal gene transfer from prokaryotes. Our results support the idea that prominent heterotrophic marine protists perform diverse functions in ocean ecology.

Original language	English (US)
Article number	310
Journal	Nature communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02235-3
State	Published - Dec 1 2018

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
General
Physics and Astronomy(all)

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10.1038/s41467-017-02235-3

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Seeleuthner, Y., Mondy, S., Lombard, V., Carradec, Q., Pelletier, E., Wessner, M., Leconte, J., Mangot, J. F., Poulain, J., Labadie, K., Logares, R., Sunagawa, S., De Berardinis, V., Salanoubat, M., Dimier, C., Kandels-Lewis, S., Picheral, M., Searson, S., Acinas, S. G., ... Wincker, P. (2018). Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans. Nature communications, 9(1), [310]. https://doi.org/10.1038/s41467-017-02235-3

Seeleuthner, Y, Mondy, S, Lombard, V, Carradec, Q, Pelletier, E, Wessner, M, Leconte, J, Mangot, JF, Poulain, J, Labadie, K, Logares, R, Sunagawa, S, De Berardinis, V, Salanoubat, M, Dimier, C, Kandels-Lewis, S, Picheral, M, Searson, S, Acinas, SG, Boss, E, Follows, M, Gorsky, G, Grimsley, N, Karp-Boss, L, Krzic, U, Not, F, Ogata, H, Raes, J, Reynaud, EG, Sardet, C, Speich, S, Stemmann, L, Velayoudon, D, Weissenbach, J, Pesant, S, Poulton, N, Stepanauskas, R, Bork, P, Bowler, C, Hingamp, P, Sullivan, MB, Iudicone, D, Massana, R, Aury, JM, Henrissat, B, Karsenti, E, Jaillon, O, Sieracki, M, De Vargas, C & Wincker, P 2018, 'Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans', Nature communications, vol. 9, no. 1, 310. https://doi.org/10.1038/s41467-017-02235-3

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title = "Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans",

abstract = "Single-celled eukaryotes (protists) are critical players in global biogeochemical cycling of nutrients and energy in the oceans. While their roles as primary producers and grazers are well appreciated, other aspects of their life histories remain obscure due to challenges in culturing and sequencing their natural diversity. Here, we exploit single-cell genomics and metagenomics data from the circumglobal Tara Oceans expedition to analyze the genome content and apparent oceanic distribution of seven prevalent lineages of uncultured heterotrophic stramenopiles. Based on the available data, each sequenced genome or genotype appears to have a specific oceanic distribution, principally correlated with water temperature and depth. The genome content provides hypotheses for specialization in terms of cell motility, food spectra, and trophic stages, including the potential impact on their lifestyles of horizontal gene transfer from prokaryotes. Our results support the idea that prominent heterotrophic marine protists perform diverse functions in ocean ecology.",

author = "Yoann Seeleuthner and Samuel Mondy and Vincent Lombard and Quentin Carradec and Eric Pelletier and Marc Wessner and Jade Leconte and Mangot, {Jean Fran{\c c}ois} and Julie Poulain and Karine Labadie and Ramiro Logares and Shinichi Sunagawa and {De Berardinis}, V{\'e}ronique and Marcel Salanoubat and C{\'e}line Dimier and Stefanie Kandels-Lewis and Marc Picheral and Sarah Searson and Acinas, {Silvia G.} and Emmanuel Boss and Michael Follows and Gabriel Gorsky and Nigel Grimsley and Lee Karp-Boss and Uros Krzic and Fabrice Not and Hiroyuki Ogata and Jeroen Raes and Reynaud, {Emmanuel G.} and Christian Sardet and Sabrina Speich and Lars Stemmann and Didier Velayoudon and Jean Weissenbach and Stephane Pesant and Nicole Poulton and Ramunas Stepanauskas and Peer Bork and Chris Bowler and Pascal Hingamp and Sullivan, {Matthew B.} and Daniele Iudicone and Ramon Massana and Aury, {Jean Marc} and Bernard Henrissat and Eric Karsenti and Olivier Jaillon and Mike Sieracki and {De Vargas}, Colomban and Patrick Wincker",

note = "Funding Information: We thank the commitment of the following people and sponsors who made this singular expedition possible: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, the French Governe-ment {\textquoteleft}Investissement d{\textquoteright}Avenir{\textquoteright} programs Oceanomics (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09), MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-11-IDEX-0001-02), Fund for Scientific Research—Flanders, VIB, Sta-zione Zoologica Anton Dohrn, UNIMIB, ANR (projects {\textquoteleft}PHYTBACK/ANR-2010-1709-01{\textquoteright}, POSEIDON/ANR-09-BLAN-0348, PROMETHEUS/ANR-09-PCS-GENM-217, TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No. 287589, IHMS/ HEALTH-F4-2010-261376), ERC Advanced Grant Award to CB (Diatomite: 294823), US NSF grant DEB-1031049 to M.E.S. and R.S., FWO, BIO5, Biosphere 2, agn{\`e}s b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L{\textquoteright}Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner and its captain and crew. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans. taraexpeditions.org). We also acknowledge C. Scarpelli for support in high-performance computing. This article is contribution number 63 of Tara Oceans. Publisher Copyright: {\textcopyright} 2018 The Author(s).",

year = "2018",

month = dec,

day = "1",

doi = "10.1038/s41467-017-02235-3",

language = "English (US)",

volume = "9",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

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TY - JOUR

T1 - Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans

AU - Seeleuthner, Yoann

AU - Mondy, Samuel

AU - Lombard, Vincent

AU - Carradec, Quentin

AU - Pelletier, Eric

AU - Wessner, Marc

AU - Leconte, Jade

AU - Mangot, Jean François

AU - Poulain, Julie

AU - Labadie, Karine

AU - Logares, Ramiro

AU - Sunagawa, Shinichi

AU - De Berardinis, Véronique

AU - Salanoubat, Marcel

AU - Dimier, Céline

AU - Kandels-Lewis, Stefanie

AU - Picheral, Marc

AU - Searson, Sarah

AU - Acinas, Silvia G.

AU - Boss, Emmanuel

AU - Follows, Michael

AU - Gorsky, Gabriel

AU - Grimsley, Nigel

AU - Karp-Boss, Lee

AU - Krzic, Uros

AU - Not, Fabrice

AU - Ogata, Hiroyuki

AU - Raes, Jeroen

AU - Reynaud, Emmanuel G.

AU - Sardet, Christian

AU - Speich, Sabrina

AU - Stemmann, Lars

AU - Velayoudon, Didier

AU - Weissenbach, Jean

AU - Pesant, Stephane

AU - Poulton, Nicole

AU - Stepanauskas, Ramunas

AU - Bork, Peer

AU - Bowler, Chris

AU - Hingamp, Pascal

AU - Sullivan, Matthew B.

AU - Iudicone, Daniele

AU - Massana, Ramon

AU - Aury, Jean Marc

AU - Henrissat, Bernard

AU - Karsenti, Eric

AU - Jaillon, Olivier

AU - Sieracki, Mike

AU - De Vargas, Colomban

AU - Wincker, Patrick

N1 - Funding Information: We thank the commitment of the following people and sponsors who made this singular expedition possible: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, the French Governe-ment ‘Investissement d’Avenir’ programs Oceanomics (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09), MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-11-IDEX-0001-02), Fund for Scientific Research—Flanders, VIB, Sta-zione Zoologica Anton Dohrn, UNIMIB, ANR (projects ‘PHYTBACK/ANR-2010-1709-01’, POSEIDON/ANR-09-BLAN-0348, PROMETHEUS/ANR-09-PCS-GENM-217, TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No. 287589, IHMS/ HEALTH-F4-2010-261376), ERC Advanced Grant Award to CB (Diatomite: 294823), US NSF grant DEB-1031049 to M.E.S. and R.S., FWO, BIO5, Biosphere 2, agnès b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L’Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner and its captain and crew. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans. taraexpeditions.org). We also acknowledge C. Scarpelli for support in high-performance computing. This article is contribution number 63 of Tara Oceans. Publisher Copyright: © 2018 The Author(s).

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Single-celled eukaryotes (protists) are critical players in global biogeochemical cycling of nutrients and energy in the oceans. While their roles as primary producers and grazers are well appreciated, other aspects of their life histories remain obscure due to challenges in culturing and sequencing their natural diversity. Here, we exploit single-cell genomics and metagenomics data from the circumglobal Tara Oceans expedition to analyze the genome content and apparent oceanic distribution of seven prevalent lineages of uncultured heterotrophic stramenopiles. Based on the available data, each sequenced genome or genotype appears to have a specific oceanic distribution, principally correlated with water temperature and depth. The genome content provides hypotheses for specialization in terms of cell motility, food spectra, and trophic stages, including the potential impact on their lifestyles of horizontal gene transfer from prokaryotes. Our results support the idea that prominent heterotrophic marine protists perform diverse functions in ocean ecology.

AB - Single-celled eukaryotes (protists) are critical players in global biogeochemical cycling of nutrients and energy in the oceans. While their roles as primary producers and grazers are well appreciated, other aspects of their life histories remain obscure due to challenges in culturing and sequencing their natural diversity. Here, we exploit single-cell genomics and metagenomics data from the circumglobal Tara Oceans expedition to analyze the genome content and apparent oceanic distribution of seven prevalent lineages of uncultured heterotrophic stramenopiles. Based on the available data, each sequenced genome or genotype appears to have a specific oceanic distribution, principally correlated with water temperature and depth. The genome content provides hypotheses for specialization in terms of cell motility, food spectra, and trophic stages, including the potential impact on their lifestyles of horizontal gene transfer from prokaryotes. Our results support the idea that prominent heterotrophic marine protists perform diverse functions in ocean ecology.

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ER -

Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans

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