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

ESF Rosenzweig and B Xu and LK Cuellar and A Martinez-Sanchez and M Schaffer and M Strauss and HN Cartwright and P Ronceray and JM Plitzko and F Forster and NS Wingreen and BD Engel and LCM Mackinder and MC Jonikas, CELL, 171, 148-+ (2017).

DOI: 10.1016/j.cell.2017.08.008

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.

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