Exploring the phycosphere of Emiliania huxleyi: From bloom dynamics to microbiome assembly experiments

Mariana Câmara dos Reis; Sarah Romac; Florence Le Gall; Dominique Marie; Miguel J. Frada; Gil Koplovitz; Thierry Cariou; Nicolas Henry; Colomban de Vargas; Christian Jeanthon

doi:10.1111/mec.16829

Exploring the phycosphere of Emiliania huxleyi: From bloom dynamics to microbiome assembly experiments

Mariana Câmara dos Reis^*, Sarah Romac, Florence Le Gall, Dominique Marie, Miguel J. Frada, Gil Koplovitz, Thierry Cariou, Nicolas Henry, Colomban de Vargas, Christian Jeanthon^*

^*Corresponding author for this work

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

1 Scopus citations

Abstract

Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. The structure and selection of prokaryotic communities associated with the most abundant coccolithophore and bloom-forming species, Emiliania huxleyi, are still poorly known. In this study, we assessed the diversity of bacterial communities associated with an E. huxleyi bloom in the Celtic Sea (Eastern North Atlantic), exposed axenic E. huxleyi cultures to prokaryotic communities derived from bloom and non-bloom conditions, and followed the dynamics of their microbiome composition over one year. Bloom-associated prokaryotic communities were dominated by SAR11, Marine group II Euryarchaeota and Rhodobacterales and contained substantial proportions of known indicators of phytoplankton bloom demises such as Flavobacteriaceae and Pseudoalteromonadaceae. The taxonomic richness of bacteria derived from natural communities associated with axenic E. huxleyi rapidly shifted and then stabilized over time. The succession of microorganisms recruited from the environment was consistently dependent on the composition of the initial bacterioplankton community. Phycosphere-associated communities derived from the E. huxleyi bloom were highly similar to one another, suggesting deterministic processes, whereas cultures from non-bloom conditions show an effect of stochasticity. Overall, this work sheds new light on the importance of the initial inoculum composition in microbiome recruitment and elucidates the temporal dynamics of its composition and long-term stability.

Original language	American English
Journal	Molecular Ecology
DOIs	https://doi.org/10.1111/mec.16829
State	Accepted/In press - 2022

Bibliographical note

Funding Information:
This work was supported by a PhD fellowship from Sorbonne University and the Région Bretagne to MCdR, the Centre National de la Recherche Scientifique (CNRS, France), the ANR grant CORALGENE (ANR‐17‐CE2‐0020‐03), and the French Government ‘‘Investissements d’Avenir’’ programmes OCEANOMICS (ANR‐11‐BTBR‐0008). We are grateful to the Tara Ocean Foundation, led by Romain Troublé and Etienne Bourgois, for the sampling opportunity and facilities onboard , and to all the scientific and logistic team involved in the Breizh Bloom cruise, notably captain Martin Herteau and his crew. We warmly thank Shai Fainsod, Michel Flores, Eric Pelletier, Daniella Schatz and Flora Vincent, for their contribution during the cruise, and Lydia White for her help in the statistical analysis. We are thankful to the Roscoff Bioinformatics platform ABiMS ( http://abims.sb‐roscoff.fr ), part of the Institut Français de Bioinformatique (ANR‐11‐INBS‐0013) and BioGenouest network, for sharing computing and storage resources, Eric Macé and INSU (Parc National d’Instrumentation Scientifique) for supplying the SBE19+ profiler, and to the RCC ( https://roscoff‐culture‐collection.org ) for providing the cultures. Tara Tara E. huxleyi

Publisher Copyright:
© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Keywords

Emiliania huxleyi
metabarcoding
microbiome assembly
phycosphere
phytoplankton–bacteria interactions

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1111/mec.16829

Cite this

@article{a84a31f8fcbe4d3ab97588dff9ba57f3,

title = "Exploring the phycosphere of Emiliania huxleyi: From bloom dynamics to microbiome assembly experiments",

abstract = "Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. The structure and selection of prokaryotic communities associated with the most abundant coccolithophore and bloom-forming species, Emiliania huxleyi, are still poorly known. In this study, we assessed the diversity of bacterial communities associated with an E. huxleyi bloom in the Celtic Sea (Eastern North Atlantic), exposed axenic E. huxleyi cultures to prokaryotic communities derived from bloom and non-bloom conditions, and followed the dynamics of their microbiome composition over one year. Bloom-associated prokaryotic communities were dominated by SAR11, Marine group II Euryarchaeota and Rhodobacterales and contained substantial proportions of known indicators of phytoplankton bloom demises such as Flavobacteriaceae and Pseudoalteromonadaceae. The taxonomic richness of bacteria derived from natural communities associated with axenic E. huxleyi rapidly shifted and then stabilized over time. The succession of microorganisms recruited from the environment was consistently dependent on the composition of the initial bacterioplankton community. Phycosphere-associated communities derived from the E. huxleyi bloom were highly similar to one another, suggesting deterministic processes, whereas cultures from non-bloom conditions show an effect of stochasticity. Overall, this work sheds new light on the importance of the initial inoculum composition in microbiome recruitment and elucidates the temporal dynamics of its composition and long-term stability.",

keywords = "Emiliania huxleyi, metabarcoding, microbiome assembly, phycosphere, phytoplankton–bacteria interactions",

author = "Mariana C{\^a}mara dos Reis and Sarah Romac and Florence Le Gall and Dominique Marie and Frada, {Miguel J.} and Gil Koplovitz and Thierry Cariou and Nicolas Henry and {de Vargas}, Colomban and Christian Jeanthon",

note = "Funding Information: This work was supported by a PhD fellowship from Sorbonne University and the R{\'e}gion Bretagne to MCdR, the Centre National de la Recherche Scientifique (CNRS, France), the ANR grant CORALGENE (ANR‐17‐CE2‐0020‐03), and the French Government {\textquoteleft}{\textquoteleft}Investissements d{\textquoteright}Avenir{\textquoteright}{\textquoteright} programmes OCEANOMICS (ANR‐11‐BTBR‐0008). We are grateful to the Tara Ocean Foundation, led by Romain Troubl{\'e} and Etienne Bourgois, for the sampling opportunity and facilities onboard , and to all the scientific and logistic team involved in the Breizh Bloom cruise, notably captain Martin Herteau and his crew. We warmly thank Shai Fainsod, Michel Flores, Eric Pelletier, Daniella Schatz and Flora Vincent, for their contribution during the cruise, and Lydia White for her help in the statistical analysis. We are thankful to the Roscoff Bioinformatics platform ABiMS ( http://abims.sb‐roscoff.fr ), part of the Institut Fran{\c c}ais de Bioinformatique (ANR‐11‐INBS‐0013) and BioGenouest network, for sharing computing and storage resources, Eric Mac{\'e} and INSU (Parc National d{\textquoteright}Instrumentation Scientifique) for supplying the SBE19+ profiler, and to the RCC ( https://roscoff‐culture‐collection.org ) for providing the cultures. Tara Tara E. huxleyi Publisher Copyright: {\textcopyright} 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.",

year = "2022",

doi = "10.1111/mec.16829",

language = "American English",

journal = "Molecular Ecology",

issn = "0962-1083",

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T1 - Exploring the phycosphere of Emiliania huxleyi

T2 - From bloom dynamics to microbiome assembly experiments

AU - Câmara dos Reis, Mariana

AU - Romac, Sarah

AU - Le Gall, Florence

AU - Marie, Dominique

AU - Frada, Miguel J.

AU - Koplovitz, Gil

AU - Cariou, Thierry

AU - Henry, Nicolas

AU - de Vargas, Colomban

AU - Jeanthon, Christian

N1 - Funding Information: This work was supported by a PhD fellowship from Sorbonne University and the Région Bretagne to MCdR, the Centre National de la Recherche Scientifique (CNRS, France), the ANR grant CORALGENE (ANR‐17‐CE2‐0020‐03), and the French Government ‘‘Investissements d’Avenir’’ programmes OCEANOMICS (ANR‐11‐BTBR‐0008). We are grateful to the Tara Ocean Foundation, led by Romain Troublé and Etienne Bourgois, for the sampling opportunity and facilities onboard , and to all the scientific and logistic team involved in the Breizh Bloom cruise, notably captain Martin Herteau and his crew. We warmly thank Shai Fainsod, Michel Flores, Eric Pelletier, Daniella Schatz and Flora Vincent, for their contribution during the cruise, and Lydia White for her help in the statistical analysis. We are thankful to the Roscoff Bioinformatics platform ABiMS ( http://abims.sb‐roscoff.fr ), part of the Institut Français de Bioinformatique (ANR‐11‐INBS‐0013) and BioGenouest network, for sharing computing and storage resources, Eric Macé and INSU (Parc National d’Instrumentation Scientifique) for supplying the SBE19+ profiler, and to the RCC ( https://roscoff‐culture‐collection.org ) for providing the cultures. Tara Tara E. huxleyi Publisher Copyright: © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

PY - 2022

Y1 - 2022

N2 - Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. The structure and selection of prokaryotic communities associated with the most abundant coccolithophore and bloom-forming species, Emiliania huxleyi, are still poorly known. In this study, we assessed the diversity of bacterial communities associated with an E. huxleyi bloom in the Celtic Sea (Eastern North Atlantic), exposed axenic E. huxleyi cultures to prokaryotic communities derived from bloom and non-bloom conditions, and followed the dynamics of their microbiome composition over one year. Bloom-associated prokaryotic communities were dominated by SAR11, Marine group II Euryarchaeota and Rhodobacterales and contained substantial proportions of known indicators of phytoplankton bloom demises such as Flavobacteriaceae and Pseudoalteromonadaceae. The taxonomic richness of bacteria derived from natural communities associated with axenic E. huxleyi rapidly shifted and then stabilized over time. The succession of microorganisms recruited from the environment was consistently dependent on the composition of the initial bacterioplankton community. Phycosphere-associated communities derived from the E. huxleyi bloom were highly similar to one another, suggesting deterministic processes, whereas cultures from non-bloom conditions show an effect of stochasticity. Overall, this work sheds new light on the importance of the initial inoculum composition in microbiome recruitment and elucidates the temporal dynamics of its composition and long-term stability.

AB - Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. The structure and selection of prokaryotic communities associated with the most abundant coccolithophore and bloom-forming species, Emiliania huxleyi, are still poorly known. In this study, we assessed the diversity of bacterial communities associated with an E. huxleyi bloom in the Celtic Sea (Eastern North Atlantic), exposed axenic E. huxleyi cultures to prokaryotic communities derived from bloom and non-bloom conditions, and followed the dynamics of their microbiome composition over one year. Bloom-associated prokaryotic communities were dominated by SAR11, Marine group II Euryarchaeota and Rhodobacterales and contained substantial proportions of known indicators of phytoplankton bloom demises such as Flavobacteriaceae and Pseudoalteromonadaceae. The taxonomic richness of bacteria derived from natural communities associated with axenic E. huxleyi rapidly shifted and then stabilized over time. The succession of microorganisms recruited from the environment was consistently dependent on the composition of the initial bacterioplankton community. Phycosphere-associated communities derived from the E. huxleyi bloom were highly similar to one another, suggesting deterministic processes, whereas cultures from non-bloom conditions show an effect of stochasticity. Overall, this work sheds new light on the importance of the initial inoculum composition in microbiome recruitment and elucidates the temporal dynamics of its composition and long-term stability.

KW - Emiliania huxleyi

KW - metabarcoding

KW - microbiome assembly

KW - phycosphere

KW - phytoplankton–bacteria interactions

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U2 - 10.1111/mec.16829

DO - 10.1111/mec.16829

M3 - Article

C2 - 36541038

AN - SCOPUS:85146988970

SN - 0962-1083

JO - Molecular Ecology

JF - Molecular Ecology

ER -

Exploring the phycosphere of Emiliania huxleyi: From bloom dynamics to microbiome assembly experiments

Abstract

Bibliographical note

Keywords

UN SDGs

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