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

Luke C. M. Mackinder, Moritz T. Meyer, Tabea Mettler-Altmann, Vivian K. Chen, Madeline C. Mitchell, Oliver Caspari, Elizabeth S. Freeman Rosenzweig, Leif Pallesen, Gregory Reeves, Alan Itakura, Robyn Roth, Frederik Sommer, Stefan Geimer, Timo Mühlhaus, Michael Schroda, Ursula Goodenough, Mark Stitt, Howard Griffiths, and Martin C. Jonikas
PNAS May 24, 2016 113 (21) 5958-5963; published ahead of print May 10, 2016 https://doi.org/10.1073/pnas.1522866113

  1. Edited by Paul G. Falkowski, Rutgers, The State University of New Jersey, New Brunswick, NJ, and approved April 7, 2016 (received for review November 20, 2015)

Significance

Eukaryotic algae, which play a fundamental role in global CO2 fixation, enhance the performance of the carbon-fixing enzyme Rubisco by placing it into an organelle called the pyrenoid. Despite the ubiquitous presence and biogeochemical importance of this organelle, how Rubisco assembles to form the pyrenoid remains a long-standing mystery. Our discovery of an abundant repeat protein that binds Rubisco in the pyrenoid represents a critical advance in our understanding of pyrenoid biogenesis. The repeat sequence of this protein suggests elegant models to explain the structural arrangement of Rubisco enzymes in the pyrenoid. Beyond advances in basic understanding, our findings open doors to the engineering of algal pyrenoids into crops to enhance yields.

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.

Footnotes

  • ↵1Present address: Cluster of Excellence in Plant Sciences and Institute of Plant Biochemistry, Heinrich-Heine University, 40225 Düsseldorf, Germany.

  • ↵2Present address: Agriculture, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT 2601, Australia.

  • ↵3Present address: Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom.

  • ↵4Present address: Institute of Molecular Biotechnology and Systems Biology, Technical University of Kaiserslautern, 67663 Kaiserslautern, Germany.

  • ↵5To whom correspondence should be addressed. Email: mjonikas{at}carnegiescience.edu.

  • Author contributions: L.C.M.M., M.T.M., T.M.-A., M. Schroda, M. Stitt, H.G., and M.C.J. designed research; L.C.M.M., M.T.M., T.M.-A., V.K.C., M.C.M., O.C., E.S.F.R., L.P., G.R., A.I., R.R., F.S., S.G., and T.M. performed research; L.C.M.M., M.T.M., T.M.-A., L.P., M. Schroda, and U.G. contributed new reagents/analytic tools; L.C.M.M., M.T.M., T.M.-A., M.C.M., F.S., S.G., T.M., and M.C.J. analyzed data; and L.C.M.M., M.T.M., T.M.-A., U.G., M. Stitt, H.G., and M.C.J. wrote the paper.

  • Conflict of interest statement: The authors wish to note that the Carnegie Institution for Science has submitted a provisional patent application on aspects of the findings.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1522866113/-/DCSupplemental.

Freely available online through the PNAS open access option.

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EPYC1 links Rubisco to form the pyrenoid
Luke C. M. Mackinder, Moritz T. Meyer, Tabea Mettler-Altmann, Vivian K. Chen, Madeline C. Mitchell, Oliver Caspari, Elizabeth S. Freeman Rosenzweig, Leif Pallesen, Gregory Reeves, Alan Itakura, Robyn Roth, Frederik Sommer, Stefan Geimer, Timo Mühlhaus, Michael Schroda, Ursula Goodenough, Mark Stitt, Howard Griffiths, Martin C. Jonikas
Proceedings of the National Academy of Sciences May 2016, 113 (21) 5958-5963; DOI: 10.1073/pnas.1522866113
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