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Cell. 2017 Sep 21;171(1):148-162.e19. doi: 10.1016/j.cell.2017.08.008.

The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization.

Author information

1
Department of Biology, Stanford University, Stanford, CA 94305, USA; Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
2
Department of Physics, Princeton University, Princeton, NJ 08544, USA.
3
Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany.
4
Cryo-EM Facility, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany.
5
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
6
Princeton Center for Theoretical Science, Princeton University, Princeton, NJ 08544, USA.
7
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA. Electronic address: wingreen@princeton.edu.
8
Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany. Electronic address: engelben@biochem.mpg.de.
9
Department of Biology, Stanford University, Stanford, CA 94305, USA; Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA. Electronic address: mjonikas@princeton.edu.

Abstract

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.

KEYWORDS:

CO(2) concentrating mechanism; Chlamydomonas reinhardtii; Rubisco; biological phase transitions; carbon fixation; cryo-electron tomography; liquid-like organelles; magic numbers; organelle inheritance; pyrenoid

PMID:
28938114
PMCID:
PMC5671343
DOI:
10.1016/j.cell.2017.08.008
[Indexed for MEDLINE]
Free PMC Article

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