Carboxysomes: cyanobacterial RubisCO comes in small packages

Abstract

Cyanobacteria (as well as many chemoautotrophs) actively pump inorganic carbon (in the form of HCO(3)(-)) into the cytosol in order to enhance the overall efficiency of carbon fixation. The success of this approach is dependent upon the presence of carboxysomes-large, polyhedral, cytosolic bodies which sequester ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO) and carbonic anhydrase. Carboxysomes seem to function by allowing ready passage of HCO(3)(-) into the body, but hindering the escape of evolved CO(2), promoting the accumulation of CO(2) in the vicinity of RubisCO and, consequently, efficient carbon fixation. This selectivity is mediated by a thin shell of protein, which envelops the carboxysome's enzymatic core and uses narrow pores to control the passage of small molecules. In this review, we summarize recent advances in understanding the organization and functioning of these intriguing, and ecologically very important molecular machines.

Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO 2 Fixation in Cyanobacteria and Some Proteobacteria

“…Further support for the hypothesis of convergent evolution is gained by the observation that the primary sequences of proteins comprising the shell structure of each type of carboxysome are more similar to the shell proteins of other types of bacterial microcompartments than to each other (108). Thus, despite their conserved functional role and their almost identical outward appearances, ␣-and ␤-carboxysomes have strikingly different internal structures.…”

“…The protein structures of CcmM-58 and CcmM-35 inform us of their specific roles within the ␤-carboxysome. The full-length CcmM-58 isoform has an N terminus with structural and primary sequence similarity to ␥-carbonic anhydrase enzymes such as Cam from Methanosarcina thermophila (108,138,139). The C terminus of CcmM-58 contains three tandem copies of a protein domain with similarity to the RubisCO small subunit (SSU-like domains) (140).…”

“…Recently, however, it emerged that the N terminus of CcmM from Thermosynechococcus elongatus BP-1 (which lacks ccaA) is a catalytically active ␥-CA enzyme (138). The ␥-CA-like domain is highly redox sensitive, suggesting once again that the carboxysome is a compartment that is inaccessible to redox equivalents-much like the way in which eukaryotic organelles operate (108). With the cytoplasm being a highly reducing environment in the light, this redox inhibition of ␥-CA activity is probably an effective adaptation, like CcaA being redox inhibited and rapidly degraded in the cytoplasm, protecting the CCM from cytoplasmic CA activity (108,138).…”

“…The ␥-CA-like domain is highly redox sensitive, suggesting once again that the carboxysome is a compartment that is inaccessible to redox equivalents-much like the way in which eukaryotic organelles operate (108). With the cytoplasm being a highly reducing environment in the light, this redox inhibition of ␥-CA activity is probably an effective adaptation, like CcaA being redox inhibited and rapidly degraded in the cytoplasm, protecting the CCM from cytoplasmic CA activity (108,138). The crystal structure of the ␥-CA-like CcmM domain forms a homotrimer (138), which is consistent with observations of trimeric CcmM behavior in carboxysomes (98).…”

Inorganic carbon utilization by aquatic photoautotrophs and potential usages of algal primary production

“…These studies have recently focused on the relationship between biochemical functions and the crystallographic structures of the carboxysome, a focal point for the CCM. Espie and Kimber (2011) and Kinney et al (2011) reviewed the role of carboxysomes in CO 2 fixation in relationship to packaging topology of CsoS1/CcmK proteins and CsoS4/CcmL proteins; respectively, these proteins form shell facets and vertices of the icosahedral body of a-and b-carboxysomes. This review also addressed key components of intracarboxysomal CO 2 formation by carbonic anhydrases and the interior organization of the carboxysome by CcmM/Cso-SCA.…”