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

Elizabeth S. Freeman Rosenzweig; Bin Xu; Luis Kuhn Cuellar; Antonio Martinez-Sanchez; Miroslava Schaffer; Mike Strauss; Heather N. Cartwright; Pierre Ronceray; Jürgen M. Plitzko; Friedrich Förster; Ned S. Wingreen; Benjamin D. Engel; Luke C.M. Mackinder; Martin C. Jonikas

doi:10.1016/j.cell.2017.08.008

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

Elizabeth S. Freeman Rosenzweig, Bin Xu, Luis Kuhn Cuellar, Antonio Martinez-Sanchez, Miroslava Schaffer, Mike Strauss, Heather N. Cartwright, Pierre Ronceray, Jürgen M. Plitzko, Friedrich Förster, Ned S. Wingreen, Benjamin D. Engel, Luke C.M. Mackinder, Martin C. Jonikas

Research output: Contribution to journal › Article › peer-review

258 Scopus citations

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.

Original language	English (US)
Pages (from-to)	148-162.e19
Journal	Cell
Volume	171
Issue number	1
DOIs	https://doi.org/10.1016/j.cell.2017.08.008
State	Published - Sep 21 2017

All Science Journal Classification (ASJC) codes

General Biochemistry, Genetics and Molecular Biology

Keywords

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

Access to Document

10.1016/j.cell.2017.08.008

Cite this

Freeman Rosenzweig, E. S., Xu, B., Kuhn Cuellar, L., Martinez-Sanchez, A., Schaffer, M., Strauss, M., Cartwright, H. N., Ronceray, P., Plitzko, J. M., Förster, F., Wingreen, N. S., Engel, B. D., Mackinder, L. C. M., & Jonikas, M. C. (2017). The Eukaryotic CO₂-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization. Cell, 171(1), 148-162.e19. https://doi.org/10.1016/j.cell.2017.08.008

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title = "The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization",

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 concentrating mechanism, Chlamydomonas reinhardtii, Rubisco, biological phase transitions, carbon fixation, cryo-electron tomography, liquid-like organelles, magic numbers, organelle inheritance, pyrenoid",

author = "{Freeman Rosenzweig}, {Elizabeth S.} and Bin Xu and {Kuhn Cuellar}, Luis and Antonio Martinez-Sanchez and Miroslava Schaffer and Mike Strauss and Cartwright, {Heather N.} and Pierre Ronceray and Plitzko, {J{\"u}rgen M.} and Friedrich F{\"o}rster and Wingreen, {Ned S.} and Engel, {Benjamin D.} and Mackinder, {Luke C.M.} and Jonikas, {Martin C.}",

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Freeman Rosenzweig, ES, Xu, B, Kuhn Cuellar, L, Martinez-Sanchez, A, Schaffer, M, Strauss, M, Cartwright, HN, Ronceray, P, Plitzko, JM, Förster, F, Wingreen, NS, Engel, BD, Mackinder, LCM & Jonikas, MC 2017, 'The Eukaryotic CO₂-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization', Cell, vol. 171, no. 1, pp. 148-162.e19. https://doi.org/10.1016/j.cell.2017.08.008

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AU - Cartwright, Heather N.

AU - Ronceray, Pierre

AU - Plitzko, Jürgen M.

AU - Förster, Friedrich

AU - Wingreen, Ned S.

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AU - Jonikas, Martin C.

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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.

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