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

• Published in: Cell 2017-09, Vol.171 (1), p.148-162.e19
• Main Authors: Freeman Rosenzweig, Elizabeth S., Xu, Bin, Kuhn Cuellar, Luis, Martinez-Sanchez, Antonio, Schaffer, Miroslava, Strauss, Mike, Cartwright, Heather N., Ronceray, Pierre, Plitzko, Jürgen M., Förster, Friedrich, Wingreen, Ned S., Engel, Benjamin D., Mackinder, Luke C.M., Jonikas, Martin C.
• Format: Article
• Language: English
• Subjects: biological phase transitions; carbon fixation; Chlamydomonas reinhardtii; CO2 concentrating mechanism; cryo-electron tomography; liquid-like organelles; magic numbers; organelle inheritance; pyrenoid; Rubisco
• ISSN: 0092-8674; 1097-4172
• 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. [Display omitted] •The pyrenoid matrix is not a crystalline solid and instead behaves like a liquid•The pyrenoid is inherited primarily by fission and can also be assembled de novo•The pyrenoid undergoes a reversible phase transition during cell division•Modeling reveals a “magic number” effect that governs phase transitions The pyrenoid, a Rubisco-containing organelle that enhances carbon fixation, mixes internally and undergoes phase transitions.