Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome

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Abstract
The carboxysome is a bacterial organelle that functions to enhance the efficiency of CO2 fixation by encapsulating the enzymes ribulose bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase. The outer shell of the carboxysome is reminiscent of a viral capsid, being constructed from many copies of a few small proteins. Here we describe the structure of the shell protein CsoS1A from the chemoautotrophic bacterium Halothiobacillus neapolitanus. The CsoS1A protein forms hexameric units that pack tightly together to form a molecular layer, which is perforated by narrow pores. Sulfate ions, soaked into crystals of CsoS1A, are observed in the pores of the molecular layer, supporting the idea that the pores could be the conduit for negatively charged metabolites such as bicarbonate, which must cross the shell. The problem of diffusion across a semiporous protein shell is discussed, with the conclusion that the shell is sufficiently porous to allow adequate transport of small molecules. The molecular layer formed by CsoS1A is similar to the recently observed layers formed by cyanobacterial carboxysome shell proteins. This similarity supports the argument that the layers observed represent the natural structure of the facets of the carboxysome shell. Insights into carboxysome function are provided by comparisons of the carboxysome shell to viral capsids, and a comparison of its pores to the pores of transmembrane protein channels. Bacterial cells are generally viewed as being relatively simple because they lack the membrane-bound organelles that help organize the interiors of eukaryotic cells. However, many bacterial cells produce large, protein-based microcompartments that serve effectively as simple organelles. These microcompartments enclose specific cellular enzymes, thereby successfully sequestering particular reactions or pathways from the rest of the cytosol. The prototypical bacterial microcompartment is the carboxysome, which is found in many bacteria that fix CO2 into organic carbon. In these bacteria, the efficiency of CO2 fixation is enhanced by having the key enzymes in that pathway encapsulated together. Carboxysomes were discovered more than 40 years ago, but an understanding of their assembly and function is just beginning to emerge. Here we report new structures of the proteins that form the outer shell of the carboxysome. These structures provide further evidence that the carboxysome shell is constructed according to principles similar to those seen in icosahedral viral capsids. The structure of the carboxysome serves as a model for understanding a variety of primitive bacterial organelles that are coming to light.

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