Bacterial Carboxysome Shell Proteins are Selectively Permeable to Carbon Fixation Substrates

Abstract

Carboxysome provides an efficient mechanism for cyanobacteria and chemoautotrophs to fix carbon dioxide (CO_2) and organic metabolites into building blocks of biomolecules. It is a polyhedral body that encapsulates ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), an enzyme that carries out the CO_2 fixation and meanwhile competitively reacts with O_2. Its outer surface is coated by the assembly of thousands of small shell proteins. Many of these shell proteins form oligomeric structures with a semi-permeable 2-3Å radius central pore, suggesting a favorable feature for the binding of anions such as bicarbonate (HCO_3-), the aqueous soluble form of CO_2. The present study examines the translocation HCO_3-, CO_2 and O_2 through the central pores of different isoforms of shell protein complexes from alpha and beta cyanobacteria. We employed umbrella sampling simulations to calculate partitioning free energy profiles of these small molecules and performed detailed electrostatic analysis of the structures. The results demonstrate that carboxysome shell protein oligomers share a unique feature in that their central pores are preferably selective for HCO_3- over hydrophobic CO_2 and O_2 gases. The pores are found to be hydrated and are electropositive, thus favoring HCO_3- and Cl- anions. Hence, as the carboxysome encapsulates carbonic anhydrase enzymes which dehydrates HCO_3- to CO_2, the preferential uptake of HCO_3-(instead of CO_2) into the carboxysomal lumen from the cytoplasm is an intrinsic way to minimize the reaction between O_2 and the RuBisCO and to increase the concentration of CO_2 around the RuBisCO. The results also provide insight into the assembled orientations of the shell proteins, which is necessary for solving a full atomic model of the carboxysome.

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