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

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

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

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    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