Volume 25, Issue 3 p. 751-765
Research Article

Widespread formation of intracellular calcium carbonates by the bloom-forming cyanobacterium Microcystis

Juliette Gaëtan

Juliette Gaëtan

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Sorbonne Université, UMR 7618 CNRS-INRA-IRD-Paris 7-UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris (iEES-Paris), Paris, France

Contribution: Conceptualization (equal), Formal analysis (equal), ​Investigation (equal), Methodology (equal), Validation (equal), Writing - original draft (equal)

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Sébastien Halary

Sébastien Halary

Muséum National d'Histoire Naturelle, UMR 7245 CNRS-MNHN, Molécules de Communication et Adaptation des Microorganismes, Paris, France

Contribution: Formal analysis (equal), Methodology (equal), Resources (equal), Validation (equal), Writing - review & editing (equal)

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Maxime Millet

Maxime Millet

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Contribution: Formal analysis (equal), ​Investigation (equal), Methodology (equal), Software (equal), Validation (equal), Visualization (equal), Writing - review & editing (equal)

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Cécile Bernard

Cécile Bernard

Muséum National d'Histoire Naturelle, UMR 7245 CNRS-MNHN, Molécules de Communication et Adaptation des Microorganismes, Paris, France

Contribution: Conceptualization (equal), Funding acquisition (equal), Writing - review & editing (equal)

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Charlotte Duval

Charlotte Duval

Muséum National d'Histoire Naturelle, UMR 7245 CNRS-MNHN, Molécules de Communication et Adaptation des Microorganismes, Paris, France

Contribution: ​Investigation (equal), Resources (equal), Writing - review & editing (equal)

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Sahima Hamlaoui

Sahima Hamlaoui

Muséum National d'Histoire Naturelle, UMR 7245 CNRS-MNHN, Molécules de Communication et Adaptation des Microorganismes, Paris, France

Contribution: Formal analysis (equal), ​Investigation (equal), Resources (equal), Validation (equal), Writing - review & editing (equal)

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Amandine Hecquet

Amandine Hecquet

Sorbonne Université, UMR 7618 CNRS-INRA-IRD-Paris 7-UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris (iEES-Paris), Paris, France

Contribution: ​Investigation (equal), Methodology (equal), Validation (equal), Writing - review & editing (equal)

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Muriel Gugger

Muriel Gugger

Institut Pasteur, Université Paris Cité, Collection of Cyanobacteria, Paris, France

Contribution: Validation (equal), Writing - review & editing (equal)

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Benjamin Marie

Benjamin Marie

Muséum National d'Histoire Naturelle, UMR 7245 CNRS-MNHN, Molécules de Communication et Adaptation des Microorganismes, Paris, France

Contribution: Conceptualization (equal), Funding acquisition (equal), Resources (equal), Writing - review & editing (equal)

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Neha Mehta

Neha Mehta

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Contribution: Formal analysis (equal), ​Investigation (equal), Writing - review & editing (equal)

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David Moreira

David Moreira

Unité d'Ecologie Systématique et Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette, France

Contribution: Conceptualization (equal), Writing - review & editing (equal)

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Fériel Skouri-Panet

Fériel Skouri-Panet

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Contribution: Conceptualization (equal), Funding acquisition (equal), ​Investigation (equal), Supervision (equal), Writing - review & editing (equal)

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Cynthia Travert

Cynthia Travert

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Contribution: ​Investigation (supporting), Methodology (supporting)

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Elodie Duprat

Elodie Duprat

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Contribution: ​Investigation (equal), Methodology (equal), Writing - review & editing (equal)

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Julie Leloup

Julie Leloup

Sorbonne Université, UMR 7618 CNRS-INRA-IRD-Paris 7-UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris (iEES-Paris), Paris, France

Contribution: Project administration (equal), Resources (equal), Supervision (equal), Writing - original draft (equal)

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Karim Benzerara

Corresponding Author

Karim Benzerara

Sorbonne Université, Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Paris, France

Correspondence

Karim Benzerara, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), Muséum National d'Histoire Naturelle, UMR CNRS-SU-MNHN 7590, Sorbonne Université, Paris, France.

Email: [email protected]

Contribution: Conceptualization (equal), Formal analysis (equal), Funding acquisition (equal), ​Investigation (equal), Methodology (equal), Project administration (equal), Supervision (equal), Writing - original draft (equal)

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First published: 22 December 2022

Funding information: Agence Nationale de la Recherche, Grant/Award Number: CE01-0005; Learning Planet Institute; and University Paris Cité grant Frontiers of Innovation in Research and Education; Muséum National d'Histoire Naturelle, ATM Program, BIOCHEMIST grant; Sorbonne Université, Emergence Program, CaCO3 project

Abstract

The formation of intracellular amorphous calcium carbonates (iACC) has been recently observed in a few cultured strains of Microcystis, a potentially toxic bloom-forming cyanobacterium found worldwide in freshwater ecosystems. If iACC-forming Microcystis are abundant within blooms, they may represent a significant amount of particulate Ca. Here, we investigate the significance of iACC biomineralization by Microcystis. First, the presence of iACC-forming Microcystis cells has been detected in several eutrophic lakes, indicating that this phenomenon occurs under environmental conditions. Second, some genotypic (presence/absence of ccyA, a marker gene of iACC biomineralization) and phenotypic (presence/absence of iACC) diversity have been detected within a collection of strains isolated from one single lake. This illustrates that this trait is frequent but also variable within Microcystis even at a single locality. Finally, one-third of publicly available genomes of Microcystis were shown to contain the ccyA gene, revealing a wide geographic and phylogenetic distribution within the genus. Overall, the present work shows that the formation of iACC by Microcystis is common under environmental conditions. While its biological function remains undetermined, this process should be further considered regarding the biology of Microcystis and implications on the Ca geochemical cycle in freshwater environments.

CONFLICT OF INTEREST

The authors declare no competing financial interest.

DATA AVAILABILITY STATEMENT

Materials described in the manuscript will be freely available upon publication of the manuscript to any researcher wishing to use them for non-commercial purposes. Genomes of the 26 PMC strains have been deposited in NCBI (BioProject ID: PRJNA888979). All other datasets generated and/or analysed during the current study (SEM/TEM) are available on the recherche.data.gouv.fr repository (doi: 10.57745/WGOJL7).