Format

Send to

Choose Destination
Proc Natl Acad Sci U S A. 2016 May 24;113(21):5958-63. doi: 10.1073/pnas.1522866113. Epub 2016 May 10.

A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle.

Author information

1
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305;
2
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom;
3
Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany;
4
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305; Department of Biology, Stanford University, Stanford, CA 94305;
5
Department of Biology, Washington University in Saint Louis, St. Louis, MO 63130;
6
Institute of Cell Biology, University of Bayreuth, 95440 Bayreuth, Germany.
7
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305; Department of Biology, Stanford University, Stanford, CA 94305; mjonikas@carnegiescience.edu.

Abstract

Biological carbon fixation is a key step in the global carbon cycle that regulates the atmosphere's composition while producing the food we eat and the fuels we burn. Approximately one-third of global carbon fixation occurs in an overlooked algal organelle called the pyrenoid. The pyrenoid contains the CO2-fixing enzyme Rubisco and enhances carbon fixation by supplying Rubisco with a high concentration of CO2 Since the discovery of the pyrenoid more that 130 y ago, the molecular structure and biogenesis of this ecologically fundamental organelle have remained enigmatic. Here we use the model green alga Chlamydomonas reinhardtii to discover that a low-complexity repeat protein, Essential Pyrenoid Component 1 (EPYC1), links Rubisco to form the pyrenoid. We find that EPYC1 is of comparable abundance to Rubisco and colocalizes with Rubisco throughout the pyrenoid. We show that EPYC1 is essential for normal pyrenoid size, number, morphology, Rubisco content, and efficient carbon fixation at low CO2 We explain the central role of EPYC1 in pyrenoid biogenesis by the finding that EPYC1 binds Rubisco to form the pyrenoid matrix. We propose two models in which EPYC1's four repeats could produce the observed lattice arrangement of Rubisco in the Chlamydomonas pyrenoid. Our results suggest a surprisingly simple molecular mechanism for how Rubisco can be packaged to form the pyrenoid matrix, potentially explaining how Rubisco packaging into a pyrenoid could have evolved across a broad range of photosynthetic eukaryotes through convergent evolution. In addition, our findings represent a key step toward engineering a pyrenoid into crops to enhance their carbon fixation efficiency.

KEYWORDS:

CO2-concentrating mechanism; Chlamydomonas reinhardtii; Rubisco; carbon fixation; pyrenoid

PMID:
27166422
PMCID:
PMC4889370
DOI:
10.1073/pnas.1522866113
[Indexed for MEDLINE]
Free PMC Article

Supplemental Content

Full text links

Icon for HighWire Icon for PubMed Central
Loading ...
Support Center