Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

被引:29
作者
Decelle, Johan [1 ,8 ]
Stryhanyuk, Hryhoriy [1 ]
Gallet, Benoit [2 ]
Veronesi, Giulia [3 ,4 ]
Schmidt, Matthias [1 ]
Balzano, Sergio [5 ,6 ]
Marro, Sophie [7 ]
Uwizeye, Clarisse [8 ]
Jouneau, Pierre-Henri [9 ]
Lupette, Josselin [8 ]
Jouhet, Juliette [8 ]
Marechal, Eric [8 ]
Schwab, Yannick [10 ]
Schieber, Nicole L. [10 ]
Tucoulou, Remi [4 ]
Richnow, Hans [1 ]
Finazzi, Giovanni [8 ]
Musat, Niculina [8 ]
机构
[1] UFZ Helmholtz Ctr Environm Res, Dept Isotope Biogeochem, D-04318 Leipzig, Germany
[2] Univ Grenoble Alpes, Inst Biol Struct, CNRS, CEA, 71 Ave Martyrs, F-38044 Grenoble, France
[3] Univ Grenoble Alpes, Lab Chim & Biol Met, UMR 5249, CNRS,CEA, 17 Ave Martyrs, F-38054 Grenoble, France
[4] ESRF, 71 Ave Martyrs, F-38043 Grenoble, France
[5] Royal Netherlands Inst Sea Res, NIOZ, Dept Marine Microbiol & Biogeochem, POB 59, NL-1790 AB Den Burg, Netherlands
[6] Univ Utrecht, POB 59, NL-1790 AB Den Burg, Netherlands
[7] UPMC Univ Paris 06, Sorbonne Univ, CNRS, Lab Oceanog Villefranche,UMR7093,Observ Oceanol, F-06 Villefranche Sur Mer, France
[8] Univ Grenoble Alpes, Cell & Plant Physiol Lab, CNRS, CEA,INRA, F-38054 Grenoble 9, France
[9] Univ Grenoble Alpes, CEA, Inst Nanosci & Cryogenie, F-38054 Grenoble, France
[10] European Mol Biol Lab, Cell Biol & Biophys Unit, D-69117 Heidelberg, Germany
关键词
ION MASS-SPECTROMETRY; X-RAY; MARINE-PHYTOPLANKTON; SULFUR ASSIMILATION; PHAEOCYSTIS BLOOMS; SURFACE WATERS; PLANT-CELLS; DIMETHYLSULFONIOPROPIONATE; PHOSPHORUS; EVOLUTION;
D O I
10.1016/j.cub.2019.01.073
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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.
引用
收藏
页码:968 / +
页数:15
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