The Eukaryotic CO 2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization

Cell. 2017 Sep 21;171(1):148-162.e19. doi: 10.1016/j.cell.2017.08.008.

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(2) concentrating mechanism; Chlamydomonas reinhardtii; Rubisco; biological phase transitions; carbon fixation; cryo-electron tomography; liquid-like organelles; magic numbers; organelle inheritance; pyrenoid.

MeSH terms

  • Algal Proteins / metabolism
  • Carbon Dioxide / metabolism
  • Chlamydomonas reinhardtii / chemistry
  • Chlamydomonas reinhardtii / cytology*
  • Chlamydomonas reinhardtii / metabolism
  • Chloroplasts / chemistry
  • Chloroplasts / metabolism
  • Chloroplasts / ultrastructure*
  • Cryoelectron Microscopy
  • Organelle Biogenesis
  • Ribulose-Bisphosphate Carboxylase / metabolism

Substances

  • Algal Proteins
  • Carbon Dioxide
  • Ribulose-Bisphosphate Carboxylase