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DOI10.1073/pnas.2025252118
Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae
Uwizeye C.; Brisbin M.M.; Gallet B.; Chevalier F.; LeKieffre C.; Schieber N.L.; Falconet D.; Wangpraseurt D.; Schertel L.; Stryhanyuk H.; Musat N.; Mitarai S.; Schwab Y.; Finazzi G.; Decelle J.
发表日期2021
ISSN0027-8424
卷号118期号:27
英文摘要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. © 2021 National Academy of Sciences. All rights reserved.
英文关键词3D electron microscopy; Oceanic plankton; Photosynthesis; Symbiosis; | single-cell transcriptomics
语种英语
来源期刊Proceedings of the National Academy of Sciences of the United States of America
文献类型期刊论文
条目标识符http://gcip.llas.ac.cn/handle/2XKMVOVA/238488
作者单位Cell and Plant Physiology Laboratory, CNRS, CEA, INRAE, IRIG, Université Grenoble Alpes, Grenoble, 38054, France; Marine Biophysics Unit, Okinawa Institute of Science and Technology Onna904-0495, Japan; Institut de Biologie Structurale, University Grenoble Alpes, CEA, CNRS, Grenoble, 38044, France; Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, 69117, Germany; Department of Nanoengineering, University of California San Diego, San Diego, CA 92903, United States; Department of Chemistry, University of Cambridge, Cambridge, CB2 1EW, United Kingdom; Scripps Institution of Oceanography, University of California San Diego, San Diego, CA 92903, United States; Department of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research-UFZ, Leipzig, 04318, Germany
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Uwizeye C.,Brisbin M.M.,Gallet B.,et al. Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae[J],2021,118(27).
APA Uwizeye C..,Brisbin M.M..,Gallet B..,Chevalier F..,LeKieffre C..,...&Decelle J..(2021).Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae.Proceedings of the National Academy of Sciences of the United States of America,118(27).
MLA Uwizeye C.,et al."Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae".Proceedings of the National Academy of Sciences of the United States of America 118.27(2021).
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