Abstract
Membraneless organelles containing the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) are a common feature of organisms utilizing CO2 concentrating mechanisms to enhance photosynthetic carbon acquisition. In cyanobacteria and proteobacteria, the Rubisco condensate is encapsulated in a proteinaceous shell, collectively termed a carboxysome, while some algae and hornworts have evolved Rubisco condensates known as pyrenoids. In both cases, CO2 fixation is enhanced compared with the free enzyme. Previous mathematical models have attributed the improved function of carboxysomes to the generation of elevated CO2 within the organelle via a colocalized carbonic anhydrase (CA) and inwardly diffusing HCO3-, which have accumulated in the cytoplasm via dedicated transporters. Here, we present a concept in which we consider the net of two protons produced in every Rubisco carboxylase reaction. We evaluate this in a reaction-diffusion compartment model to investigate functional advantages these protons may provide Rubisco condensates and carboxysomes, prior to the evolution of HCO3- accumulation. Our model highlights that diffusional resistance to reaction species within a condensate allows Rubisco-derived protons to drive the conversion of HCO3- to CO2 via colocalized CA, enhancing both condensate [CO2] and Rubisco rate. Protonation of Rubisco substrate (RuBP) and product (phosphoglycerate) plays an important role in modulating internal pH and CO2 generation. Application of the model to putative evolutionary ancestors, prior to contemporary cellular HCO3- accumulation, revealed photosynthetic enhancements along a logical sequence of advancements, via Rubisco condensation, to fully formed carboxysomes. Our model suggests that evolution of Rubisco condensation could be favored under low CO2 and low light environments.
Highlights
Bisphosphate carboxylase/oxygenase (Rubisco) are a common feature of organisms utilizing CO2 concentrating mechanisms to enhance photosynthetic carbon acquisition
Previous mathematical models have attributed the improved function of carboxysomes to the generation of elevated CO2 within the organelle via a colocalized carbonic anhydrase (CA) and inwardly diffusing HCO3−, which have accumulated in the cytoplasm via dedicated transporters
The Rubisco oxygenation reaction has increased, to the detriment of CO2 capture. This catalytic paradox has led to different adaptive solutions to ensure effective rates of photosynthetic CO2 fixation including the evolution of the kinetic properties of the enzyme (4), increases in Rubisco abundance in the leaves of many terrestrial C3 plants (5), and the evolution of diverse and complex CO2 concentrating mechanisms (CCMs) in Rubisco is arguably the most abundant protein on Earth, and its catalytic action is responsible for the bulk of organic carbon in the biosphere
Summary
Bisphosphate carboxylase/oxygenase (Rubisco) are a common feature of organisms utilizing CO2 concentrating mechanisms to enhance photosynthetic carbon acquisition. A defining characteristic of contemporary cyanobacteria is the encapsulation of their Rubisco enzymes within specialized, proteinencased microcompartments called carboxysomes (8) These microbodies are central to the cyanobacterial CCM, in which cellular bicarbonate (HCO3−) is elevated by a combination of membraneassociated HCO3− pumps and CO2-to-HCO3− converting complexes (9–11), to drive CO2 production within the carboxysome by an internal carbonic anhydrase (CA; 12, 13). Our model shows that proton production via Rubisco reactions, and those carried by protonated reaction species, can enable the elevation of condensate CO2 to enhance carboxylation Application of this theory provides insights into pyrenoid and carboxysome evolution. D.F.S. is a guest editor invited by the Editorial Board
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