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 journalArticle

51 Citations (Scopus)

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 languageEnglish (US)
Pages (from-to)148-162.e19
JournalCell
Volume171
Issue number1
DOIs
StatePublished - Sep 21 2017

Fingerprint

Organelles
Algae
Liquids
Ribulose-Bisphosphate Carboxylase
Crystalline materials
Chlamydomonas reinhardtii
Chloroplasts
Phase separation
Cell Division
Cells
Enzymes

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)

Keywords

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

Cite this

Freeman Rosenzweig, E. S., Xu, B., Kuhn Cuellar, L., Martinez-Sanchez, A., Schaffer, M., Strauss, 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
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. / The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization. In: Cell. 2017 ; Vol. 171, No. 1. pp. 148-162.e19.
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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

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

In: Cell, Vol. 171, No. 1, 21.09.2017, p. 148-162.e19.

Research output: Contribution to journalArticle

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AU - Freeman Rosenzweig, Elizabeth S.

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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.

PY - 2017/9/21

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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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Freeman Rosenzweig ES, Xu B, Kuhn Cuellar L, Martinez-Sanchez A, Schaffer M, Strauss M et al. The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization. Cell. 2017 Sep 21;171(1):148-162.e19. https://doi.org/10.1016/j.cell.2017.08.008