Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

Type : ACL
Nature : Production scientifique
Au bénéfice du Laboratoire : Oui
Statut de publication : Publié
Année de publication : 2019
Auteurs (18) : DECELLE Johan STRYHANYUK Hryhoriy GALLET Benoit VERONESI Giulia SCHMIDT Matthias BALZANO Sergio MARRO Sophie UWIZEYE Clarisse JOUNEAU Pierre-henri LUPETTE Josselin JOUHET Juliette MARÉCHAL Eric SCHWAB Yannick SCHIEBER Nicole,l TUCOULOU Rémi RICHNOW Hans FINAZZI Giovanni MUSAT Niculina
Revue scientifique : Current Biology
Volume : 29
Fascicule : 6
Pages : 968-978
DOI : 10.1016/j.cub.2019.01.073
URL : http://www.sciencedirect.com/science/article/pii/s0960982219301320
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.
Mots-clés : symbiosis; plankton; microalga; single-cell imaging; photosynthesis; mass spectrometry imaging; 3D electron microscopy; eukaryotes; plastid; Phaeocystis
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Citation :
Decelle J, Stryhanyuk H, Gallet B, Veronesi G, Schmidt M, Balzano S, Marro S, Uwizeye C, Jouneau P-H, 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. Curr Biol 29: 968-978 | doi: 10.1016/j.cub.2019.01.073