Comparative analysis of carboxysome shell proteins

Abstract

Carboxysomes are metabolic modules for CO 2 fixation that are found in all cyanobacteria and some chemoautotrophic bacteria. They comprise a semi-permeable proteinaceous shell that encapsulates ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase. Structural studies are revealing the integral role of the shell protein paralogs to carboxysome form and function. The shell proteins are composed of two domain classes: those with the bacterial microcompartment (BMC; Pfam00936) domain, which oligomerize to form (pseudo)hexamers, and those with the CcmL/EutN (Pfam03319) domain which form pentamers in carboxysomes. These two shell protein types are proposed to be the basis for the carboxysome's icosahedral geometry. The shell proteins are also thought to allow the flux of metabolites across the shell through the presence of the small pore formed by their hexameric/pentameric symmetry axes. In this review, we describe bioinformatic and structural analyses that highlight the important primary, tertiary, and quaternary structural features of these conserved shell subunits. In the future, further understanding of these molecular building blocks may provide the basis for enhancing CO 2 fixation in other organisms or creating novel biological nanostructures.

pH determines the energetic efficiency of the cyanobacterial CO 2 concentrating mechanism

“…This assumption is supported by measurements of millimolar RuBP in S. elongatus (37), but it remains unclear how RuBP enters the carboxysome (49,56). Similarly, we assume that O 2 enters the carboxysome quickly enough to equalize concentrations across the carboxysome shell (SI Appendix), that is, that the CCM is not an "oxygen-blocking mechanism.…”

“…Throughout the text, we assumed that the carboxysome is equally permeable to CO 2 and HCO 3 − . However, recent structures of carboxysome shell proteins offer a potential mechanism for differential permeability of CO 2 and HCO 3 − : The pores of shell proteins typically carry positive charge, which might increase the rate of HCO 3 − transit relative to CO 2 (12,49). Indeed, recent experimental evidence suggests that protein compartments can be selectively permeable (50,51).…”

“…However, it is not known whether HCO 3 − , H 2 CO 3 , and CO 3 2− are equally permeable to the carboxysome. As mentioned above, pores on the carboxysome shell often carry positive charge, so it is plausible that charge would affect the rate substrates enter the carboxysome (12,49). Direct measurement of the permeability characteristics of the carboxysome would be of great help in understanding the CCM.…”

The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment

“…Both ␣-and ␤-types of carboxysome shells contain a minor component, CsoS4 or CcmL, respectively, that belongs to the EutN domain family (pfam03319); CsoS4 and CcmL form pentamers proposed to serve as the vertices of the icosahedron (1,3).…”

“…A recent bioinformatic survey revealed that ϳ20% of sequenced bacterial genomes, from 13 bacterial phyla, have genes coding for both protein families, suggesting that the potential for forming compartments enclosed by carboxysome-like shells is widespread in the bacterial domain (11). The functions of some of these have been experimentally determined (12)(13)(14)(15), but for most the only available functional information is derived from the annotations of the genes clustering with shell protein genes (3,11). Collectively, carboxysomes and these (presumably) architecturally similar organelles are known as BMCs.…”