Abstract
Carboxysomes are bacterial microcompartments that enhance carbon fixation by concentrating ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and its substrate CO2 within a proteinaceous shell. They are found in all cyanobacteria, some purple photoautotrophs and many chemoautotrophic bacteria. Carboxysomes consist of a protein shell that encapsulates several hundred molecules of RuBisCO, and contain carbonic anhydrase and other accessory proteins. Genes coding for carboxysome shell components and the encapsulated proteins are typically found together in an operon. The α-carboxysome operon is embedded in a cluster of additional, conserved genes that are presumably related to its function. In many chemoautotrophs, products of the expanded carboxysome locus include CbbO and CbbQ, a member of the AAA+ domain superfamily. We bioinformatically identified subtypes of CbbQ proteins and show that their genes frequently co-occur with both Form IA and Form II RuBisCO. The α-carboxysome-associated ortholog, CsoCbbQ, from Halothiobacillus neapolitanus forms a hexamer in solution and hydrolyzes ATP. The crystal structure shows that CsoCbbQ is a hexamer of the typical AAA+ domain; the additional C-terminal domain, diagnostic of the CbbQ subfamily, structurally fills the inter-monomer gaps, resulting in a distinctly hexagonal shape. We show that CsoCbbQ interacts with CsoCbbO and is a component of the carboxysome shell, the first example of ATPase activity associated with a bacterial microcompartment.
Highlights
Anhydrase; this effectively elevates the substrate concentration near the active site of RuBisCO
Genes encoding α -carboxysome components constitute an operon, the cso operon[11,12], which in H. nea includes the genes for the Form IA RuBisCO large and small subunits, the large shell protein CsoS2 that is essential for carboxysome assembly[13], the shell-associated β -carbonic anhydrase CsoSCA14, the pentameric CsoS4A and CsoS4B proteins that form the vertices of the carboxysome shell[15,16], and the hexameric shell subunit assemblies of CsoS1A, CsoS1B, CsoS1C (Fig. 1a)[12]
The CbbQ orthologs fall into four classes: those encoded proximal to the genes for 1) non-carboxysomal Form IA RuBisCO, 2) Form II RuBisCO, 3) the α -carboxysome superlocus
Summary
Anhydrase; this effectively elevates the substrate concentration near the active site of RuBisCO. Its gene product was recently identified as a potential α -carboxysome RuBisCO assembly factor; it improved recombinant RuBisCO solubility when co-expressed with the GroEL/ES chaperonin complex in E. coli[20] The need for such assembly factors for proper RuBisCO folding in plants and cyanobacteria is well documented; presumably they are required in chemoautotrophs as well[21,22]. Another member of the expanded α -carboxysome locus is CbbQ, a member of the AAA+ superfamily proteins (ATPases Associated with diverse cellular Activities), which are found across all kingdoms of life and fulfill a variety of functions, mostly involved in ATP-driven dissociation, unfolding and remodeling of macromolecules[23,24]. The effect of CbbQ on the carboxysomal RuBisCO and on carboxysome function is unknown
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