Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds

Andrea Del Cortona (Lead / Corresponding author), Christopher J. Jackson, François Bucchini, Michiel Van Bel, Sofie D'hondt, Pavel Škaloud, Charles F. Delwiche, Andrew H. Knoll, John A. Raven, Heroen Verbruggen, Klaas Vandepoele (Lead / Corresponding author), Olivier De Clerck (Lead / Corresponding author), Frederik Leliaert (Lead / Corresponding author)

    Research output: Contribution to journalArticle

    Abstract

    The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focuses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified in benthic environments that became increasingly available as ice retreated. An increased supply of nutrients and biotic interactions, such as grazing pressure, likely triggered the independent evolution of macroscopic growth via different strategies, including true multicellularity, and multiple types of giant-celled forms.

    Original languageEnglish
    Pages (from-to)2551-2559
    Number of pages9
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume117
    Issue number5
    Early online date7 Jan 2020
    DOIs
    Publication statusPublished - 4 Feb 2020

    Fingerprint

    Seaweed
    Ecosystem
    Growth
    Chlorophyta
    Ice
    Giant Cells
    Fresh Water
    Climate
    Oceans and Seas
    Radiation
    Pressure
    Food

    Keywords

    • green algae
    • Chlorophyta
    • phylogenomics
    • phylogeny
    • Ulvophyceae

    Cite this

    Del Cortona, Andrea ; Jackson, Christopher J. ; Bucchini, François ; Van Bel, Michiel ; D'hondt, Sofie ; Škaloud, Pavel ; Delwiche, Charles F. ; Knoll, Andrew H. ; Raven, John A. ; Verbruggen, Heroen ; Vandepoele, Klaas ; De Clerck, Olivier ; Leliaert, Frederik. / Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds. In: Proceedings of the National Academy of Sciences of the United States of America. 2020 ; Vol. 117, No. 5. pp. 2551-2559.
    @article{753b0a4c8b734b7ebd57994d1bbd212a,
    title = "Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds",
    abstract = "The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focuses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified in benthic environments that became increasingly available as ice retreated. An increased supply of nutrients and biotic interactions, such as grazing pressure, likely triggered the independent evolution of macroscopic growth via different strategies, including true multicellularity, and multiple types of giant-celled forms.",
    keywords = "green algae, Chlorophyta, phylogenomics, phylogeny, Ulvophyceae",
    author = "{Del Cortona}, Andrea and Jackson, {Christopher J.} and Fran{\cc}ois Bucchini and {Van Bel}, Michiel and Sofie D'hondt and Pavel Škaloud and Delwiche, {Charles F.} and Knoll, {Andrew H.} and Raven, {John A.} and Heroen Verbruggen and Klaas Vandepoele and {De Clerck}, Olivier and Frederik Leliaert",
    note = "This work was supported by Ghent University (BOF/01J04813) with infrastructure funded by European Marine Biological Resource Centre Belgium/Research Foundation - Flanders Project GOH3817N (to O.D.C.); the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant agreement H2020-MSCA-ITN-2015-675752; the Australian Research Council Grant DP150100705 (to H.V.); the Maryland Agricultural Experiment Station; and the National Science Foundation GRAToL 10136495 (to C.F.D.). The University of Dundee is a registered Scottish charity, No. 050196.",
    year = "2020",
    month = "2",
    day = "4",
    doi = "10.1073/pnas.1910060117",
    language = "English",
    volume = "117",
    pages = "2551--2559",
    journal = "Proceedings of the National Academy of Sciences",
    issn = "0027-8424",
    publisher = "National Academy of Sciences",
    number = "5",

    }

    Del Cortona, A, Jackson, CJ, Bucchini, F, Van Bel, M, D'hondt, S, Škaloud, P, Delwiche, CF, Knoll, AH, Raven, JA, Verbruggen, H, Vandepoele, K, De Clerck, O & Leliaert, F 2020, 'Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, no. 5, pp. 2551-2559. https://doi.org/10.1073/pnas.1910060117

    Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds. / Del Cortona, Andrea (Lead / Corresponding author); Jackson, Christopher J.; Bucchini, François; Van Bel, Michiel; D'hondt, Sofie; Škaloud, Pavel; Delwiche, Charles F.; Knoll, Andrew H.; Raven, John A.; Verbruggen, Heroen; Vandepoele, Klaas (Lead / Corresponding author); De Clerck, Olivier (Lead / Corresponding author); Leliaert, Frederik (Lead / Corresponding author).

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, No. 5, 04.02.2020, p. 2551-2559.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds

    AU - Del Cortona, Andrea

    AU - Jackson, Christopher J.

    AU - Bucchini, François

    AU - Van Bel, Michiel

    AU - D'hondt, Sofie

    AU - Škaloud, Pavel

    AU - Delwiche, Charles F.

    AU - Knoll, Andrew H.

    AU - Raven, John A.

    AU - Verbruggen, Heroen

    AU - Vandepoele, Klaas

    AU - De Clerck, Olivier

    AU - Leliaert, Frederik

    N1 - This work was supported by Ghent University (BOF/01J04813) with infrastructure funded by European Marine Biological Resource Centre Belgium/Research Foundation - Flanders Project GOH3817N (to O.D.C.); the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant agreement H2020-MSCA-ITN-2015-675752; the Australian Research Council Grant DP150100705 (to H.V.); the Maryland Agricultural Experiment Station; and the National Science Foundation GRAToL 10136495 (to C.F.D.). The University of Dundee is a registered Scottish charity, No. 050196.

    PY - 2020/2/4

    Y1 - 2020/2/4

    N2 - The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focuses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified in benthic environments that became increasingly available as ice retreated. An increased supply of nutrients and biotic interactions, such as grazing pressure, likely triggered the independent evolution of macroscopic growth via different strategies, including true multicellularity, and multiple types of giant-celled forms.

    AB - The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focuses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified in benthic environments that became increasingly available as ice retreated. An increased supply of nutrients and biotic interactions, such as grazing pressure, likely triggered the independent evolution of macroscopic growth via different strategies, including true multicellularity, and multiple types of giant-celled forms.

    KW - green algae

    KW - Chlorophyta

    KW - phylogenomics

    KW - phylogeny

    KW - Ulvophyceae

    UR - http://www.scopus.com/inward/record.url?scp=85079021543&partnerID=8YFLogxK

    U2 - 10.1073/pnas.1910060117

    DO - 10.1073/pnas.1910060117

    M3 - Article

    C2 - 31911467

    VL - 117

    SP - 2551

    EP - 2559

    JO - Proceedings of the National Academy of Sciences

    JF - Proceedings of the National Academy of Sciences

    SN - 0027-8424

    IS - 5

    ER -