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Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

By Johan Decelle, Hryhoriy Stryhanyuk, Benoit Gallet, Giulia Veronesi, Matthias Schmidt, Sergio Balzano, Sophie Marro, Clarisse Uwizeye, Pierre-Henri Jouneau, Josselin Lupette, Juliette Jouhet, Eric Maréchal, Yannick Schwab, Nicole Schieber, Rémi Tucoulou, Hans Richnow, Giovanni Finazzi and Niculina Musat

Abstract

International audiencePhotosymbiosis between single-celled hosts and microalgae is common in oceanic plankton, especially in oligotrophic surface waters. However, the functioning of this ecologically important cell-cell interaction and the subcellular mechanisms allowing the host to accommodate and benefit from its microalgae remain enigmatic. Here, using a combination of quantitative single-cell structural and chemical imaging techniques (FIB-SEM, nanoSIMS, Synchrotron X-ray fluorescence), we show that the structural organization, physiology, and trophic status of the algal symbionts (the haptophyte Phaeocystis) significantly change within their acantharian hosts compared to their free-living phase in culture. In symbiosis, algal cell division is blocked, photosynthesis is enhanced, and cell volume is increased by up to 10-fold with a higher number of plastids (from 2 to up to 30) and thylakoid membranes. The multiplication of plastids can lead to a 38-fold increase of the total plastid volume in a cell. Subcellular mapping of nutrients (nitrogen and phosphorous) and their stoichiometric ratios shows that symbiotic algae are impoverished in phosphorous and suggests a higher investment in energy-acquisition machinery rather than in growth. Nanoscale imaging also showed that the host supplies a substantial amount of trace metals (e.g., iron and cobalt), which are stored in algal vacuoles at high concentrations (up to 660 ppm). Sulfur mapping reveals a high concentration in algal vacuoles that may be a source of antioxidant molecules. Overall, this study unveils an unprecedented morphological and metabolic transformation of microalgae following their integration into a host, and it suggests that this widespread symbiosis is a farming strategy wherein the host engulfs and exploits microalgae

Topics: single-cell imaging, Phaeocystis, eukaryotes, mass spectrometry imaging, microalga, photosynthesis, Metal homeostasis, symbiosis, plastid, plankton, 3D electron microscopy, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Publisher: 'Elsevier BV'
Year: 2019
DOI identifier: 10.1016/j.cub.2019.01.073
OAI identifier: oai:HAL:hal-02083159v1
Provided by: HAL-INSU
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