Effects of microcompartmentation on flux distribution and metabolic pools in Chlamydomonas reinhardtii chloroplasts

Elife. 2018 Oct 11:7:e37960. doi: 10.7554/eLife.37960.

Abstract

Cells and organelles are not homogeneous but include microcompartments that alter the spatiotemporal characteristics of cellular processes. The effects of microcompartmentation on metabolic pathways are however difficult to study experimentally. The pyrenoid is a microcompartment that is essential for a carbon concentrating mechanism (CCM) that improves the photosynthetic performance of eukaryotic algae. Using Chlamydomonas reinhardtii, we obtained experimental data on photosynthesis, metabolites, and proteins in CCM-induced and CCM-suppressed cells. We then employed a computational strategy to estimate how fluxes through the Calvin-Benson cycle are compartmented between the pyrenoid and the stroma. Our model predicts that ribulose-1,5-bisphosphate (RuBP), the substrate of Rubisco, and 3-phosphoglycerate (3PGA), its product, diffuse in and out of the pyrenoid, respectively, with higher fluxes in CCM-induced cells. It also indicates that there is no major diffusional barrier to metabolic flux between the pyrenoid and stroma. Our computational approach represents a stepping stone to understanding microcompartmentalized CCM in other organisms.

Keywords: Chlamydomonas reinhardtii; biochemistry; carbon fixation; chemical biology; chlamydomonas reinhardtii; mathematical model; microcompartment; plant biology; pyrenoid; systems modeling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Carbon
  • Carbon Cycle / drug effects
  • Carbon Dioxide / pharmacology
  • Cell Compartmentation*
  • Chlamydomonas reinhardtii / drug effects
  • Chlamydomonas reinhardtii / enzymology
  • Chlamydomonas reinhardtii / growth & development
  • Chlamydomonas reinhardtii / metabolism*
  • Chloroplasts / drug effects
  • Chloroplasts / metabolism*
  • Metabolic Flux Analysis*
  • Metabolome
  • Models, Biological
  • Photosynthesis / drug effects

Substances

  • Carbon Dioxide
  • Carbon