@article {uwizeye_cytoklepty_2021, title = {Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae}, journal = {Proceedings of the National Academy of Sciences}, volume = {118}, number = {27}, year = {2021}, note = {Publisher: National Academy of Sciences Section: Biological Sciences}, month = {jul}, abstract = {Endosymbioses have shaped the evolutionary trajectory of life and remain ecologically important. Investigating oceanic photosymbioses can illuminate how algal endosymbionts are energetically exploited by their heterotrophic hosts and inform on putative initial steps of plastid acquisition in eukaryotes. By combining three-dimensional subcellular imaging with photophysiology, carbon flux imaging, and transcriptomics, we show that cell division of endosymbionts (Phaeocystis) is blocked within hosts (Acantharia) and that their cellular architecture and bioenergetic machinery are radically altered. Transcriptional evidence indicates that a nutrient-independent mechanism prevents symbiont cell division and decouples nuclear and plastid division. As endosymbiont plastids proliferate, the volume of the photosynthetic machinery volume increases 100-fold in correlation with the expansion of a reticular mitochondrial network in close proximity to plastids. Photosynthetic efficiency tends to increase with cell size, and photon propagation modeling indicates that the networked mitochondrial architecture enhances light capture. This is accompanied by 150-fold higher carbon uptake and up-regulation of genes involved in photosynthesis and carbon fixation, which, in conjunction with a ca.15-fold size increase of pyrenoids demonstrates enhanced primary production in symbiosis. Mass spectrometry imaging revealed major carbon allocation to plastids and transfer to the host cell. As in most photosymbioses, microalgae are contained within a host phagosome (symbiosome), but here, the phagosome invaginates into enlarged microalgal cells, perhaps to optimize metabolic exchange. This observation adds evidence that the algal metamorphosis is irreversible. Hosts, therefore, trigger and benefit from major bioenergetic remodeling of symbiotic microalgae with potential consequences for the oceanic carbon cycle. Unlike other photosymbioses, this interaction represents a so-called cytoklepty, which is a putative initial step toward plastid acquisition.}, keywords = {3D electron microscopy, oceanic plankton, Photosynthesis, rcc, rcc1383, single-cell transcriptomics, symbiosis}, issn = {0027-8424, 1091-6490}, doi = {10.1073/pnas.2025252118}, url = {https://www.pnas.org/content/118/27/e2025252118}, author = {Uwizeye, Clarisse and Brisbin, Margaret Mars and Gallet, Benoit and Chevalier, Fabien and LeKieffre, Charlotte and Schieber, Nicole L. and Falconet, Denis and Wangpraseurt, Daniel and Schertel, Lukas and Stryhanyuk, Hryhoriy and Musat, Niculina and Mitarai, Satoshi and Schwab, Yannick and Finazzi, Giovanni and Decelle, Johan} } @article {uwizeye_morphological_2021, title = {Morphological bases of phytoplankton energy management and physiological responses unveiled by 3D subcellular imaging}, journal = {Nature Communications}, volume = {12}, number = {1}, year = {2021}, note = {Number: 1 Publisher: Nature Publishing Group}, month = {feb}, pages = {1{\textendash}12}, abstract = {Phytoplankton account for a large proportion of global primary production and comprise a number of phylogenetically distinct lineages. Here, Uwizeye et al. use FIB-SEM to study ultrastructural plasticity of 7 distinct taxa and describe how subcellular organisation is linked to energy metabolism.}, keywords = {RCC100, RCC4014, RCC827, RCC909}, issn = {2041-1723}, doi = {10.1038/s41467-021-21314-0}, url = {http://www.nature.com/articles/s41467-021-21314-0}, author = {Uwizeye, Clarisse and Decelle, Johan and Jouneau, Pierre-Henri and Flori, Serena and Gallet, Benoit and Keck, Jean-baptiste and Bo, Davide Dal and Moriscot, Christine and Seydoux, Claire and Chevalier, Fabien and Schieber, Nicole L. and Templin, Rachel and Allorent, Guillaume and Courtois, Florence and Curien, Gilles and Schwab, Yannick and Schoehn, Guy and Zeeman, Samuel C. and Falconet, Denis and Finazzi, Giovanni} } @article {decelle_subcellular_2021, title = {Subcellular architecture and metabolic connection in the planktonic photosymbiosis between Collodaria (radiolarians) and their microalgae}, journal = {bioRxiv}, year = {2021}, note = {Company: Cold Spring Harbor Laboratory Distributor: Cold Spring Harbor Laboratory Label: Cold Spring Harbor Laboratory Section: New Results Type: article}, pages = {2021.03.13.435225}, abstract = {Photosymbiosis is widespread and ecologically important in the oceanic plankton but remains poorly studied. Here, we used multimodal subcellular imaging to investigate the photosymbiosis between colonial Collodaria and their microalga dinoflagellate (Brandtodinium) collected in surface seawaters. We showed that this symbiosis is a very dynamic system whereby symbionts interact with different host cells via extracellular vesicles within the {\textquotedblleft}greenhouse-like{\textquotedblright} colony. 3D electron microscopy revealed that the volume of the photosynthetic apparatus (plastid and pyrenoid) of the microalgae increased in symbiosis compared to free-living while the mitochondria volume was similar. Stable isotope probing coupled with NanoSIMS showed that carbon and nitrogen were assimilated and stored in the symbiotic microalga in starch granules and purine crystals, respectively. Nitrogen was also allocated to the algal nucleus (nucleolus). After 3 hours, low 13C and 15N transfer was detected in the host Golgi. Metal mapping revealed that intracellular iron concentration was similar in free-living and symbiotic microalgae (ca 40 ppm) and two-fold higher in the host, whereas copper concentration increased in symbiotic microalgae (up to 6900 ppm) and was detected in the host cell and extracellular vesicles. Sulfur mapping also pinpointed the importance of this nutrient for the algal metabolism. This study, which revealed subcellular changes of the morphology and nutrient homeostasis in symbiotic microalgae, improves our understanding on the metabolism of this widespread and abundant oceanic symbiosis and paves the way for more studies to investigate the metabolites exchanged.}, doi = {10.1101/2021.03.13.435225}, url = {https://www.biorxiv.org/content/10.1101/2021.03.13.435225v1}, author = {Decelle, Johan and Veronesi, Giulia and LeKieffre, Charlotte and Gallet, Benoit and Chevalier, Fabien and Stryhanyuk, Hryhoriy and Marro, Sophie and Ravanel, St{\'e}phane and Tucoulou, R{\'e}mi and Schieber, Nicole and Finazzi, Giovanni and Schwab, Yannick and Musat, Niculina} } @article {Uwizeye2020, title = {In-cell quantitative structural imaging of phytoplankton using 3D electron microscopy}, journal = {bioRxiv}, year = {2020}, note = {tex.mendeley-tags: RCC100,RCC4014,RCC827,RCC909}, month = {jan}, pages = {2020.05.19.104166}, abstract = {Phytoplankton is a minor fraction of the global biomass playing a major role in primary production and climate. Despite improved understanding of phytoplankton diversity and genomics, we lack nanoscale subcellular imaging approaches to understand their physiology and cell biology. Here, we present a complete Focused Ion Beam - Scanning Electron Microscopy (FIB-SEM) workflow (from sample preparation to image processing) to generate nanometric 3D phytoplankton models. Tomograms of entire cells, representatives of six ecologically-successful phytoplankton unicellular eukaryotes, were used for quantitative morphometric analysis. Besides lineage-specific cellular architectures, we observed common features related to cellular energy management: i) conserved cell-volume fractions occupied by the different organelles; ii) consistent plastid-mitochondria interactions, iii) constant volumetric ratios in these energy-producing organelles. We revealed detailed subcellular features related to chromatin organization and to biomineralization. Overall, this approach opens new perspectives to study phytoplankton acclimation responses to abiotic and biotic factors at a relevant biological scale.Competing Interest StatementThe authors have declared no competing interest.}, keywords = {RCC100, RCC4014, RCC827, RCC909}, doi = {10.1101/2020.05.19.104166}, url = {http://biorxiv.org/content/early/2020/05/20/2020.05.19.104166.abstract}, author = {Uwizeye, Clarisse and Decelle, Johan and Jouneau, Pierre-Henri and Gallet, Benoit and Keck, Jean-baptiste and Schwab, Yannick and Schoehn, Guy and Zeeman, Samuel C and Falconet, Denis and Finazzi, Giovanni and Moriscot, Christine and Chevalier, Fabien and Schieber, Nicole L and Templin, Rachel and Curien, Gilles and Schwab, Yannick and Schoehn, Guy and Zeeman, Samuel C and Falconet, Denis and Finazzi, Giovanni} } @article {Decelle2019, title = {Algal remodeling in a ubiquitous planktonic photosymbiosis}, journal = {Current Biology}, volume = {29}, number = {6}, year = {2019}, note = {Publisher: Cell Press tex.mendeley-tags: RCC1719}, month = {mar}, pages = {968{\textendash}978.e4}, 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 = {RCC1719}, issn = {0960-9822}, doi = {10.1016/J.CUB.2019.01.073}, url = {https://www.sciencedirect.com/science/article/abs/pii/S0960982219301320$\#$undfig1}, author = {Decelle, Johan and Stryhanyuk, Hryhoriy and Gallet, Benoit and Veronesi, Giulia and Schmidt, Matthias and Balzano, Sergio and Marro, Sophie and Uwizeye, Clarisse and Jouneau, Pierre-Henri and Lupette, Josselin and Jouhet, Juliette and Mar{\'e}chal, {\'E}ric and Schwab, Yannick and Schieber, Nicole L. and Tucoulou, R{\'e}mi and Richnow, Hans and Finazzi, Giovanni and Musat, Niculina} }