TY - JOUR
T1 - The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization
AU - Freeman Rosenzweig, Elizabeth S.
AU - Xu, Bin
AU - Kuhn Cuellar, Luis
AU - Martinez-Sanchez, Antonio
AU - Schaffer, Miroslava
AU - Strauss, Mike
AU - Cartwright, Heather N.
AU - Ronceray, Pierre
AU - Plitzko, Jürgen M.
AU - Förster, Friedrich
AU - Wingreen, Ned S.
AU - Engel, Benjamin D.
AU - Mackinder, Luke C.M.
AU - Jonikas, Martin C.
N1 - Funding Information:
We thank W. Baumeister, J. Berry, D. Ehrhardt, J. Feldman, W. Frommer, A. Grossman, Y. Meir, M.B. Mudgett, M. Scott, H. Stone, V. Walbot, and members of the Jonikas laboratory for helpful discussion and suggestions, and we thank U. Goodenough, A. Grossman, A. McCormick, and M.T. Meyer for critical reading of the manuscript. This work was supported by the National Science Foundation ( EF-1105617 and IOS-1359682 to M.C.J. and PHY-1305525 to N.S.W.), the Carnegie Institution for Science (to L.C.M.M. and M.C.J.); NIH ( T32GM007276 to E.S.F.R. and 7DP2GM119137-02 to M.C.J.), the Simons Foundation and HHMI ( 55108535 ), and Princeton University (to M.C.J.), a CONACyT-DAAD Graduate Scholarship (to L.K.C), a Fundación Séneca Postdoctoral Fellowship (to A.M.-S.), an Alexander von Humboldt Foundation Postdoctoral Fellowship (to B.D.E), and the Deutsche Forschungsgemeinschaft ( FO 716/4-1 to F.F.).
Publisher Copyright:
© 2017 Elsevier Inc.
PY - 2017/9/21
Y1 - 2017/9/21
N2 - Approximately 30%–40% of global CO2 fixation occurs inside a non-membrane-bound organelle called the pyrenoid, which is found within the chloroplasts of most eukaryotic algae. The pyrenoid matrix is densely packed with the CO2-fixing enzyme Rubisco and is thought to be a crystalline or amorphous solid. Here, we show that the pyrenoid matrix of the unicellular alga Chlamydomonas reinhardtii is not crystalline but behaves as a liquid that dissolves and condenses during cell division. Furthermore, we show that new pyrenoids are formed both by fission and de novo assembly. Our modeling predicts the existence of a “magic number” effect associated with special, highly stable heterocomplexes that influences phase separation in liquid-like organelles. This view of the pyrenoid matrix as a phase-separated compartment provides a paradigm for understanding its structure, biogenesis, and regulation. More broadly, our findings expand our understanding of the principles that govern the architecture and inheritance of liquid-like organelles.
AB - Approximately 30%–40% of global CO2 fixation occurs inside a non-membrane-bound organelle called the pyrenoid, which is found within the chloroplasts of most eukaryotic algae. The pyrenoid matrix is densely packed with the CO2-fixing enzyme Rubisco and is thought to be a crystalline or amorphous solid. Here, we show that the pyrenoid matrix of the unicellular alga Chlamydomonas reinhardtii is not crystalline but behaves as a liquid that dissolves and condenses during cell division. Furthermore, we show that new pyrenoids are formed both by fission and de novo assembly. Our modeling predicts the existence of a “magic number” effect associated with special, highly stable heterocomplexes that influences phase separation in liquid-like organelles. This view of the pyrenoid matrix as a phase-separated compartment provides a paradigm for understanding its structure, biogenesis, and regulation. More broadly, our findings expand our understanding of the principles that govern the architecture and inheritance of liquid-like organelles.
KW - CO concentrating mechanism
KW - Chlamydomonas reinhardtii
KW - Rubisco
KW - biological phase transitions
KW - carbon fixation
KW - cryo-electron tomography
KW - liquid-like organelles
KW - magic numbers
KW - organelle inheritance
KW - pyrenoid
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U2 - 10.1016/j.cell.2017.08.008
DO - 10.1016/j.cell.2017.08.008
M3 - Article
C2 - 28938114
AN - SCOPUS:85029607410
SN - 0092-8674
VL - 171
SP - 148-162.e19
JO - Cell
JF - Cell
IS - 1
ER -