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

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.

SUBMITTER: Mackinder LC

PROVIDER: S-EPMC4889370 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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

Mackinder Luke C M LC Meyer Moritz T MT Mettler-Altmann Tabea T Chen Vivian K VK Mitchell Madeline C MC Caspari Oliver O Freeman Rosenzweig Elizabeth S ES Pallesen Leif L Reeves Gregory G Itakura Alan A Roth Robyn R Sommer Frederik F Geimer Stefan S Mühlhaus Timo T Schroda Michael M Goodenough Ursula U Stitt Mark M Griffiths Howard H Jonikas Martin C MC

Proceedings of the National Academy of Sciences of the United States of America 20160510 21

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 bi ...[more]

PMID: 27166422

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Project description:Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO) is the carbon-fixing enzyme present in most photosynthetic organisms, converting CO2 into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO2 and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C4 photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO2 concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O2. The energy efficiency of C3 photosynthesis, from which the C4 pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO2. Part of the homeostatic mechanism that maintains this constancy of supply involves the CO2 produced as a byproduct of photorespiration in a negative feedback loop. Analyzing the database of RuBisCO kinetic parameters, we suggest that in genera (Flaveria and Panicum) for which both C3 and C4 examples are available, the C4 pathway evolved only from C3 ancestors possessing much lower than the average carboxylase specificity relative to that of the oxygenase reaction (S C/O=S C/S O), and hence, the higher CO2 levels required for development of the photorespiratory CO2 pump (C2 photosynthesis) essential in the initial stages of C4 evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO2 turnover may have occurred, which would have been supported by the higher CO2 levels. Otherwise, C4 RuBisCO kinetic traits remain little changed from the ancestral C3 species. At the opposite end of the spectrum, C3 plants (from Limonium) with higher than average S C/O, which may be associated with the ability of increased CO2, relative to O2, affinity to offset reduced photorespiration and chloroplast CO2 levels, can tolerate high stress environments. It is suggested that, instead of inherently constrained by its kinetic mechanism, RuBisCO possesses the extensive kinetic plasticity necessary for adaptation to changes in photorespiration that occur in the homeostatic regulation of CO2 supply under a broad range of abiotic environmental conditions.

Dataset Information

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

Publications

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

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