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Variable inter and intraspecies alkaline phosphatase activity within single cells of revived dinoflagellates

Abstract

Adaptation of cell populations to environmental changes is mediated by phenotypic variability at the single-cell level. Enzyme activity is a key factor in cell phenotype and the expression of the alkaline phosphatase activity (APA) is a fundamental phytoplankton strategy for maintaining growth under phosphate-limited conditions. Our aim was to compare the APA among cells and species revived from sediments of the Bay of Brest (Brittany, France), corresponding to a pre-eutrophication period (1940’s) and a beginning of a post-eutrophication period (1990’s) during which phosphate concentrations have undergone substantial variations. Both toxic marine dinoflagellate Alexandrium minutum and the non-toxic dinoflagellate Scrippsiella acuminata were revived from ancient sediments. Using microfluidics, we measured the kinetics of APA at the single-cell level. Our results indicate that all S. acuminata strains had significantly higher APA than A. minutum strains. For both species, the APA in the 1990’s decade was significantly lower than in the 1940’s. For the first time, our results reveal both inter and intraspecific variabilities of dinoflagellate APA and suggest that, at a half-century timescale, two different species of dinoflagellate may have undergone similar adaptative evolution to face environmental changes and acquire ecological advantages.

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Fig. 1: Sampling area and the six dinoflagellate strains revivifed from the sediment core.
Fig. 2: Examples of the six strains of dinoflagellates having alkaline phosphatase activity (APA).
Fig. 3: Variability of the alkaline phosphatase activity (APA) for two strains of Scrippsiella acuminata (SC-47–1; SC-92–1) as a function of time.
Fig. 4: Difference in the maximum alkaline phosphatase activity (APA) of the Scrippsiella acuminata (SC) and Alexandrium minutum (AM) strains.

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Acknowledgements

We thank the Syndicat de bassin d’Elorn for providing the historical data of nitrate and phosphate concentrations. MG, JCB and YDA acknowledge financial support of a Marie-Curie Individual Fellowships (IF) MAPAPAIMA (797007). JCB acknowledges the financial support of the Region Nouvelle Aquitaine and from the French state in the frame of the ‘investment for the future’ (Programme IdEx Bordeaux, ANR-10-IDEX-03–02). Revived cultures and culture experiments were carried out in the frame of the project PALMIRA part of the project PALMIRA (Palaeoecology of Alexandrium minutum dans la Rade de Brest–Marché n°2017–90292) financed by the Région Brittany. We are grateful to all members of the crew of the N/O Thalia ship of Ifremer for providing technical expertise in sediment core collection and to Emulseo for providing the surfactant used in this study. We thank Prof. Josh D. Neufeld and anonymous reviewers for their valuable comments and insights that considerably helped to improve the manuscript.

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MG, JCB and RS conceived and designed the study (MG, JCB microfluidics; MG, RS microbiology). Experiments were performed by MG (APA experiments, microfluidics), CL (phosphate concentrations measurements) and ML (cultivation and preparation of cells) under the supervision of RS and JCB. MG, LB and TB contributed analytical tools (MG, LB microfluidic platform and instrumentation; MG, TB microfluidic chips, MG image processing). MG, CL, CJ, YDA and JCB contributed to data analysis. MG, JCB and RS wrote the manuscript with contributions from all authors.

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Correspondence to Raffaele Siano or Jean-Christophe Baret.

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JCB is a co-founder of Emulseo whose surfactant formulation was used in this study.

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Girault, M., Siano, R., Labry, C. et al. Variable inter and intraspecies alkaline phosphatase activity within single cells of revived dinoflagellates. ISME J 15, 2057–2069 (2021). https://doi.org/10.1038/s41396-021-00904-2

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