Insights into the Evolution of Multicellularity from the Sea Lettuce Genome

Olivier De Clerck (Lead / Corresponding author), Shu-Min Kao, Kenny A. Bogaert, Jonas Blomme, Fatima Foflonker, Michiel Kwantes, Emmelien Vancaester, Lisa Vanderstraeten, Eylem Aydogdu, Jens Boesger, Gianmaria Califano, Benedicte Charrier, Rachel Clewes, Andrea Del Cortona, Sofie D'Hondt, Noe Fernandez-Pozo, Claire M. Gachon, Marc Hanikenne, Linda Lattermann, Frederik Leliaert & 16 others Xiaojie Liu, Christine A. Maggs, Zoë A. Popper, John A. Raven, Michiel Van Bel, Per K. I. Wilhelmsson, Debashish Bhattacharya, Juliet C. Coates, Stefan A. Rensing, Dominique Van Der Straeten, Assaf Vardi, Lieven Sterck, Klaas Vandepoele, Yves Van de Peer, Thomas Wichard, John H. Bothwell

    Research output: Contribution to journalArticle

    3 Citations (Scopus)

    Abstract

    We report here the 98.5 Mbp haploid genome (12,924 protein coding genes) of Ulva mutabilis, a ubiquitous and iconic representative of the Ulvophyceae or green seaweeds. Ulva's rapid and abundant growth makes it a key contributor to coastal biogeochemical cycles; its role in marine sulfur cycles is particularly important because it produces high levels of dimethylsulfoniopropionate (DMSP), the main precursor of volatile dimethyl sulfide (DMS). Rapid growth makes Ulva attractive biomass feedstock but also increasingly a driver of nuisance “green tides.” Ulvophytes are key to understanding the evolution of multicellularity in the green lineage, and Ulva morphogenesis is dependent on bacterial signals, making it an important species with which to study cross-kingdom communication. Our sequenced genome informs these aspects of ulvophyte cell biology, physiology, and ecology. Gene family expansions associated with multicellularity are distinct from those of freshwater algae. Candidate genes, including some that arose following horizontal gene transfer from chromalveolates, are present for the transport and metabolism of DMSP. The Ulva genome offers, therefore, new opportunities to understand coastal and marine ecosystems and the fundamental evolution of the green lineage. De Clerck et al. present the first genome sequence of a green seaweed, a dominant group of primary producers in coastal environments. The Ulva genome informs on an independent acquisition of multicellularity, sheds light on adaptations to life in intertidal habitats, and identifies candidate genes involved in DMSP biosynthesis and conversion to DMS.

    Original languageEnglish
    Pages (from-to)2921-2933.e5
    Number of pages13
    JournalCurrent Biology
    Volume28
    Issue number18
    Early online date13 Aug 2018
    DOIs
    Publication statusPublished - 24 Sep 2018

    Fingerprint

    Ulva
    Genes
    Genome
    genome
    dimethyl sulfide
    Seaweed
    algae
    Ecosystem
    macroalgae
    genes
    Ocular Adaptation
    Cell Physiological Phenomena
    Horizontal Gene Transfer
    Haploidy
    Growth
    Ecology
    feedstocks
    Fresh Water
    Morphogenesis
    Sulfur

    Keywords

    • DMS
    • DMSP
    • green seaweeds
    • multicellularity
    • phytohormones
    • Ulva

    Cite this

    De Clerck, O., Kao, S-M., Bogaert, K. A., Blomme, J., Foflonker, F., Kwantes, M., ... Bothwell, J. H. (2018). Insights into the Evolution of Multicellularity from the Sea Lettuce Genome. Current Biology, 28(18), 2921-2933.e5. https://doi.org/10.1016/j.cub.2018.08.015
    De Clerck, Olivier ; Kao, Shu-Min ; Bogaert, Kenny A. ; Blomme, Jonas ; Foflonker, Fatima ; Kwantes, Michiel ; Vancaester, Emmelien ; Vanderstraeten, Lisa ; Aydogdu, Eylem ; Boesger, Jens ; Califano, Gianmaria ; Charrier, Benedicte ; Clewes, Rachel ; Del Cortona, Andrea ; D'Hondt, Sofie ; Fernandez-Pozo, Noe ; Gachon, Claire M. ; Hanikenne, Marc ; Lattermann, Linda ; Leliaert, Frederik ; Liu, Xiaojie ; Maggs, Christine A. ; Popper, Zoë A. ; Raven, John A. ; Van Bel, Michiel ; Wilhelmsson, Per K. I. ; Bhattacharya, Debashish ; Coates, Juliet C. ; Rensing, Stefan A. ; Van Der Straeten, Dominique ; Vardi, Assaf ; Sterck, Lieven ; Vandepoele, Klaas ; Van de Peer, Yves ; Wichard, Thomas ; Bothwell, John H. / Insights into the Evolution of Multicellularity from the Sea Lettuce Genome. In: Current Biology. 2018 ; Vol. 28, No. 18. pp. 2921-2933.e5.
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    abstract = "We report here the 98.5 Mbp haploid genome (12,924 protein coding genes) of Ulva mutabilis, a ubiquitous and iconic representative of the Ulvophyceae or green seaweeds. Ulva's rapid and abundant growth makes it a key contributor to coastal biogeochemical cycles; its role in marine sulfur cycles is particularly important because it produces high levels of dimethylsulfoniopropionate (DMSP), the main precursor of volatile dimethyl sulfide (DMS). Rapid growth makes Ulva attractive biomass feedstock but also increasingly a driver of nuisance “green tides.” Ulvophytes are key to understanding the evolution of multicellularity in the green lineage, and Ulva morphogenesis is dependent on bacterial signals, making it an important species with which to study cross-kingdom communication. Our sequenced genome informs these aspects of ulvophyte cell biology, physiology, and ecology. Gene family expansions associated with multicellularity are distinct from those of freshwater algae. Candidate genes, including some that arose following horizontal gene transfer from chromalveolates, are present for the transport and metabolism of DMSP. The Ulva genome offers, therefore, new opportunities to understand coastal and marine ecosystems and the fundamental evolution of the green lineage. De Clerck et al. present the first genome sequence of a green seaweed, a dominant group of primary producers in coastal environments. The Ulva genome informs on an independent acquisition of multicellularity, sheds light on adaptations to life in intertidal habitats, and identifies candidate genes involved in DMSP biosynthesis and conversion to DMS.",
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    note = "esearch support was provided by NERC grant NBAF925 and BBSRC grant BB:K020552 (to C.A.M. and J.H.B.), UGent Special Research FundBOF/01J04813 (to O.D.C. and K.V.), BOF/GOA 01G01715 (to K.V. and E.V), and BOF/01SC2316 (to X.L.) with infrastructure funded by EMBRC Belgium—FWO project GOH3817N (to O.D.C.), EU Horizon2020 Marie Curie ITN ALFF-Project642575 (to C.M.G., O.D.C., T.W., G.C., and Y.V.d.P.), German Research Foundation CRC ChemBioSys1127 (to T.W., J. Boesger, M.K., G.C., and L.L.), Postdoctoral Fellowship Grant of the Research Foundation—Flanders (to J. Blomme—project 12T3418N), BBSRC-funded MIBTP PhD rotation project (to R.C. and J.C.C.), United States Department of EnergyDE-EE0003373/001 (to D.B.), and National Science Foundation IGERT for Renewable and Sustainable Fuels program 0903675 (to F.F.). M.H. is research associate of the FNRS. We thank Dr. Severin Sasso (University Jena) for providing T.W. with the real-time PCR detection system. This publication is based upon work from COST Action FA1406 PHYCOMORPH (to B.C., J.C.C, J.H.B., O.D.C., S.A.R., and T.W.), supported by COST (European Cooperation in Science and Technology).",
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    De Clerck, O, Kao, S-M, Bogaert, KA, Blomme, J, Foflonker, F, Kwantes, M, Vancaester, E, Vanderstraeten, L, Aydogdu, E, Boesger, J, Califano, G, Charrier, B, Clewes, R, Del Cortona, A, D'Hondt, S, Fernandez-Pozo, N, Gachon, CM, Hanikenne, M, Lattermann, L, Leliaert, F, Liu, X, Maggs, CA, Popper, ZA, Raven, JA, Van Bel, M, Wilhelmsson, PKI, Bhattacharya, D, Coates, JC, Rensing, SA, Van Der Straeten, D, Vardi, A, Sterck, L, Vandepoele, K, Van de Peer, Y, Wichard, T & Bothwell, JH 2018, 'Insights into the Evolution of Multicellularity from the Sea Lettuce Genome', Current Biology, vol. 28, no. 18, pp. 2921-2933.e5. https://doi.org/10.1016/j.cub.2018.08.015

    Insights into the Evolution of Multicellularity from the Sea Lettuce Genome. / De Clerck, Olivier (Lead / Corresponding author); Kao, Shu-Min; Bogaert, Kenny A.; Blomme, Jonas; Foflonker, Fatima; Kwantes, Michiel; Vancaester, Emmelien; Vanderstraeten, Lisa; Aydogdu, Eylem; Boesger, Jens; Califano, Gianmaria; Charrier, Benedicte; Clewes, Rachel; Del Cortona, Andrea; D'Hondt, Sofie; Fernandez-Pozo, Noe; Gachon, Claire M.; Hanikenne, Marc; Lattermann, Linda; Leliaert, Frederik; Liu, Xiaojie; Maggs, Christine A.; Popper, Zoë A.; Raven, John A.; Van Bel, Michiel; Wilhelmsson, Per K. I.; Bhattacharya, Debashish; Coates, Juliet C.; Rensing, Stefan A.; Van Der Straeten, Dominique; Vardi, Assaf; Sterck, Lieven; Vandepoele, Klaas; Van de Peer, Yves; Wichard, Thomas; Bothwell, John H. (Lead / Corresponding author).

    In: Current Biology, Vol. 28, No. 18, 24.09.2018, p. 2921-2933.e5.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Insights into the Evolution of Multicellularity from the Sea Lettuce Genome

    AU - De Clerck, Olivier

    AU - Kao, Shu-Min

    AU - Bogaert, Kenny A.

    AU - Blomme, Jonas

    AU - Foflonker, Fatima

    AU - Kwantes, Michiel

    AU - Vancaester, Emmelien

    AU - Vanderstraeten, Lisa

    AU - Aydogdu, Eylem

    AU - Boesger, Jens

    AU - Califano, Gianmaria

    AU - Charrier, Benedicte

    AU - Clewes, Rachel

    AU - Del Cortona, Andrea

    AU - D'Hondt, Sofie

    AU - Fernandez-Pozo, Noe

    AU - Gachon, Claire M.

    AU - Hanikenne, Marc

    AU - Lattermann, Linda

    AU - Leliaert, Frederik

    AU - Liu, Xiaojie

    AU - Maggs, Christine A.

    AU - Popper, Zoë A.

    AU - Raven, John A.

    AU - Van Bel, Michiel

    AU - Wilhelmsson, Per K. I.

    AU - Bhattacharya, Debashish

    AU - Coates, Juliet C.

    AU - Rensing, Stefan A.

    AU - Van Der Straeten, Dominique

    AU - Vardi, Assaf

    AU - Sterck, Lieven

    AU - Vandepoele, Klaas

    AU - Van de Peer, Yves

    AU - Wichard, Thomas

    AU - Bothwell, John H.

    N1 - esearch support was provided by NERC grant NBAF925 and BBSRC grant BB:K020552 (to C.A.M. and J.H.B.), UGent Special Research FundBOF/01J04813 (to O.D.C. and K.V.), BOF/GOA 01G01715 (to K.V. and E.V), and BOF/01SC2316 (to X.L.) with infrastructure funded by EMBRC Belgium—FWO project GOH3817N (to O.D.C.), EU Horizon2020 Marie Curie ITN ALFF-Project642575 (to C.M.G., O.D.C., T.W., G.C., and Y.V.d.P.), German Research Foundation CRC ChemBioSys1127 (to T.W., J. Boesger, M.K., G.C., and L.L.), Postdoctoral Fellowship Grant of the Research Foundation—Flanders (to J. Blomme—project 12T3418N), BBSRC-funded MIBTP PhD rotation project (to R.C. and J.C.C.), United States Department of EnergyDE-EE0003373/001 (to D.B.), and National Science Foundation IGERT for Renewable and Sustainable Fuels program 0903675 (to F.F.). M.H. is research associate of the FNRS. We thank Dr. Severin Sasso (University Jena) for providing T.W. with the real-time PCR detection system. This publication is based upon work from COST Action FA1406 PHYCOMORPH (to B.C., J.C.C, J.H.B., O.D.C., S.A.R., and T.W.), supported by COST (European Cooperation in Science and Technology).

    PY - 2018/9/24

    Y1 - 2018/9/24

    N2 - We report here the 98.5 Mbp haploid genome (12,924 protein coding genes) of Ulva mutabilis, a ubiquitous and iconic representative of the Ulvophyceae or green seaweeds. Ulva's rapid and abundant growth makes it a key contributor to coastal biogeochemical cycles; its role in marine sulfur cycles is particularly important because it produces high levels of dimethylsulfoniopropionate (DMSP), the main precursor of volatile dimethyl sulfide (DMS). Rapid growth makes Ulva attractive biomass feedstock but also increasingly a driver of nuisance “green tides.” Ulvophytes are key to understanding the evolution of multicellularity in the green lineage, and Ulva morphogenesis is dependent on bacterial signals, making it an important species with which to study cross-kingdom communication. Our sequenced genome informs these aspects of ulvophyte cell biology, physiology, and ecology. Gene family expansions associated with multicellularity are distinct from those of freshwater algae. Candidate genes, including some that arose following horizontal gene transfer from chromalveolates, are present for the transport and metabolism of DMSP. The Ulva genome offers, therefore, new opportunities to understand coastal and marine ecosystems and the fundamental evolution of the green lineage. De Clerck et al. present the first genome sequence of a green seaweed, a dominant group of primary producers in coastal environments. The Ulva genome informs on an independent acquisition of multicellularity, sheds light on adaptations to life in intertidal habitats, and identifies candidate genes involved in DMSP biosynthesis and conversion to DMS.

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    KW - multicellularity

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    De Clerck O, Kao S-M, Bogaert KA, Blomme J, Foflonker F, Kwantes M et al. Insights into the Evolution of Multicellularity from the Sea Lettuce Genome. Current Biology. 2018 Sep 24;28(18):2921-2933.e5. https://doi.org/10.1016/j.cub.2018.08.015