Decelle 2019 Curr Biol

Decelle J, Stryhanyuk H, Gallet B, Veronesi G, Schmidt M, Balzano S, Marro S, Uwizeye C, Jouneau PH, Lupette J, Jouhet J, Maréchal E, Schwab Y, Schieber NL, Tucoulou R, Richnow H, Finazzi G, Musat N (2019) Algal remodeling in a ubiquitous planktonic photosymbiosis. https://doi.org/10.1016/j.cub.2019.01.073

» Curr Biol 29:968-78.e4. PMID: 30827917 Open Access

Decelle Johan, Stryhanyuk Hryhoriy, Gallet Benoit, Veronesi Giulia, Schmidt Matthias, Balzano Sergio, Marro Sophie, Uwizeye Clarisse, Jouneau Pierre-Henri, Lupette Josselin, Jouhet Juliette, Marechal Eric, Schwab Yannick, Schieber Nicole L, Tucoulou Remi, Richnow Hans, Finazzi Giovanni, Musat Niculina (2019) Curr Biol

Abstract: Photosymbiosis 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. • Keywords: 3D electron microscopy, Phaeocystis, Eukaryotes, Mass spectrometry imaging, Microalga, Photosynthesis, Plankton, Plastid, Single-cell imaging, Symbiosis • Bioblast editor: Plangger M

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