Algal remodeling in a ubiquitous planktonic photosymbiosis
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, N.L.; Tucoulou, R.; Richnow, H.; Finazzi, G.; Musat, N. (2019). Algal remodeling in a ubiquitous planktonic photosymbiosis. Curr. Biol. 29(6): 968-978.e4. https://dx.doi.org/10.1016/j.cub.2019.01.073 In: Current Biology. Cell Press: London. ISSN 0960-9822; e-ISSN 1879-0445, more |  |
| Keyword | Phaeocystis Lagerheim, 1893 [WoRMS]
| | Author keywords | symbiosis; plankton; microalga; single-cell imaging; photosynthesis; mass spectrometry imaging; 3D electron microscopy; eukaryotes; plastid; Phaeocystis |
| Authors | | Top | - Decelle, J.
- Stryhanyuk, H.
- Gallet, B.
- Veronesi, G.
- Schmidt, M.
- Balzano, S., more
| - Marro, S.
- Uwizeye, C.
- Jouneau, P.-H.
- Lupette, J.
- Jouhet, J.
- Maréchal, E.
| - Schwab, Y.
- Schieber, N.L.
- Tucoulou, R.
- Richnow, H.
- Finazzi, G.
- Musat, N.
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| 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. |
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