Phosphorus starvation induces membrane remodeling and recycling in Emiliania huxleyi

被引:67
作者
Shemi, Adva [1 ]
Schatz, Daniella [1 ]
Fredricks, Helen F. [2 ]
Van Mooy, Benjamin A. S. [2 ]
Porat, Ziv [3 ]
Vardi, Assaf [1 ]
机构
[1] Weizmann Inst Sci, Dept Plant & Environm Sci, IL-7610001 Rehovot, Israel
[2] Woods Hole Oceanog Inst, Dept Marine Chem & Geochem, Woods Hole, MA 02543 USA
[3] Weizmann Inst Sci, Biol Serv Dept, IL-7610001 Rehovot, Israel
基金
欧洲研究理事会;
关键词
alkaline phosphatase; autophagy; cell size; coccolithophores; lipid substitution; membrane vesicles; phosphate stress; phospholipids; PROGRAMMED CELL-DEATH; ALKALINE-PHOSPHATASE; MOLECULAR-MECHANISMS; P-LIMITATION; VIRUS; 86; AUTOPHAGY; PHYTOPLANKTON; COCCOLITHOPHORE; INFECTION; NITROGEN;
D O I
10.1111/nph.13940
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Nutrient availability is an important factor controlling phytoplankton productivity. Phytoplankton contribute c. 50% of the global photosynthesis and possess efficient acclimation mechanisms to cope with nutrient stress. We investigate the cellular response of the bloom-forming coccolithophore Emiliania huxleyi to phosphorus (P) scarcity, which is often a limiting factor in marine ecosystems. We combined mass spectrometry, fluorescence microscopy, transmission electron microscopy (TEM) and gene expression analyses in order to assess diverse cellular features in cells exposed to P limitation and recovery. Early starvation-induced substitution of phospholipids in the cells' membranes with galacto- and betaine lipids. Lipid remodeling was rapid and reversible upon P resupply. The PI3K inhibitor wortmannin reduced phospholipid substitution, suggesting a possible involvement of PI3K- signaling in this process. In addition, P limitation enhanced the formation and acidification of membrane vesicles in the cytoplasm. Intracellular vesicles may facilitate the recycling of cytoplasmic content, which is engulfed in the vesicles and delivered to the main vacuole. Long-term starvation was characterized by a profound increase in cell size and morphological alterations in cellular ultrastructure. This study provides cellular and molecular basis for future ecophysiological assessment of natural E.huxleyi populations in oligotrophic regions.
引用
收藏
页码:886 / 898
页数:13
相关论文
共 80 条
  • [1] Membrane Glycerolipid Remodeling Triggered by Nitrogen and Phosphorus Starvation in Phaeodactylum tricornutum
    Abida, Heni
    Dolch, Lina-Juana
    Mei, Coline
    Villanova, Valeria
    Conte, Melissa
    Block, Maryse A.
    Finazzi, Giovanni
    Bastien, Olivier
    Tirichine, Leila
    Bowler, Chris
    Rebeille, Fabrice
    Petroutsos, Dimitris
    Jouhet, Juliette
    Marechal, Eric
    [J]. PLANT PHYSIOLOGY, 2015, 167 (01) : 118 - 136
  • [2] Identification of the algal dimethyl sulfide-releasing enzyme: A missing link in the marine sulfur cycle
    Alcolombri, Uria
    Ben-Dor, Shifra
    Feldmesser, Ester
    Levin, Yishai
    Tawfik, Dan S.
    Vardi, Assaf
    [J]. SCIENCE, 2015, 348 (6242) : 1466 - 1469
  • [3] Balch WM, 2004, COCCOLITHOPHORES: FROM MOLECULAR PROCESSES TO GLOBAL IMPACT, P165
  • [4] Enslavement in the Water Body by Toxic Aphanizomenon ovalisporum, Inducing Alkaline Phosphatase in Phytoplanktons
    Bar-Yosef, Yehonathan
    Sukenik, Assaf
    Hadas, Ora
    Viner-Mozzini, Yehudit
    Kaplan, Aaron
    [J]. CURRENT BIOLOGY, 2010, 20 (17) : 1557 - 1561
  • [5] Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export
    Bar-Zeev, Edo
    Avishay, Itamar
    Bidle, Kay D.
    Berman-Frank, Ilana
    [J]. ISME JOURNAL, 2013, 7 (12) : 2340 - 2348
  • [6] Climate-driven trends in contemporary ocean productivity
    Behrenfeld, Michael J.
    O'Malley, Robert T.
    Siegel, David A.
    McClain, Charles R.
    Sarmiento, Jorge L.
    Feldman, Gene C.
    Milligan, Allen J.
    Falkowski, Paul G.
    Letelier, Ricardo M.
    Boss, Emmanuel S.
    [J]. NATURE, 2006, 444 (7120) : 752 - 755
  • [7] ACCUMULATION OF A NOVEL GLYCOLIPID AND A BETAINE LIPID IN CELLS OF RHODOBACTER-SPHAEROIDES GROWN UNDER PHOSPHATE LIMITATION
    BENNING, C
    HUANG, ZH
    GAGE, DA
    [J]. ARCHIVES OF BIOCHEMISTRY AND BIOPHYSICS, 1995, 317 (01) : 103 - 111
  • [8] Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi
    Bidle, Kay D.
    Haramaty, Liti
    Barcelos e Ramos, Joana
    Falkowski, Paul
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (14) : 6049 - 6054
  • [9] The Molecular Ecophysiology of Programmed Cell Death in Marine Phytoplankton
    Bidle, Kay D.
    [J]. ANNUAL REVIEW OF MARINE SCIENCE, VOL 7, 2015, 7 : 341 - 375
  • [10] Billard C, 2004, COCCOLITHOPHORES: FROM MOLECULAR PROCESSES TO GLOBAL IMPACT, P1