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

Abstract

SUMMARY Cyanobacteria are the globally dominant photoautotrophic lineage. Their success is dependent on a set of adaptations collectively termed the CO 2 -concentrating mechanism (CCM). The purpose of the CCM is to support effective CO 2 fixation by enhancing the chemical conditions in the vicinity of the primary CO 2 -fixing enzyme, d -ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO), to promote the carboxylase reaction and suppress the oxygenase reaction. In cyanobacteria and some proteobacteria, this is achieved by encapsulation of RubisCO within carboxysomes, which are examples of a group of proteinaceous bodies called bacterial microcompartments. Carboxysomes encapsulate the CO 2 -fixing enzyme within the selectively permeable protein shell and simultaneously encapsulate a carbonic anhydrase enzyme for CO 2 supply from a cytoplasmic bicarbonate pool. These bodies appear to have arisen twice and undergone a process of convergent evolution. While the gross structures of all known carboxysomes are ostensibly very similar, with shared gross features such as a selectively permeable shell layer, each type of carboxysome encapsulates a phyletically distinct form of RubisCO enzyme. Furthermore, the specific proteins forming structures such as the protein shell or the inner RubisCO matrix are not identical between carboxysome types. Each type has evolutionarily distinct forms of the same proteins, as well as proteins that are entirely unrelated to one another. In light of recent developments in the study of carboxysome structure and function, we present this review to summarize the knowledge of the structure and function of both types of carboxysome. We also endeavor to cast light on differing evolutionary trajectories which may have led to the differences observed in extant carboxysomes.

Intracellular Ca-carbonate biomineralization is widespread in cyanobacteria

“…The formation of amorphous Ca-carbonate inclusions requires relatively high supersaturation conditions (33), suggesting that relatively high concentrations of Ca 2+ and/or CO 3 2-must prevail in the cytoplasm of intracellularly Cacarbonate biomineralizing cyanobacteria. In general, some local increase in the concentration of CO 3 2-may be expected close to carboxysomes from which OH − are released to the cytoplasm by the conversion of HCO 3 − to CO 2 by carboxysomal carbonic anhydrases (34). Intracellular calcification may occur in cyanobacteria regulating less efficiently their intracellular pH.…”

Ecology and biogeochemistry of cyanobacteria in soils, permafrost, aquatic and cryptic polar habitats

“…In any event, cyanobacteria have been shown to use a number of methods in order to increase photosynthesis (Rae et al 2013). For example, they are able to produce carboxysomes, which together with CO 2 -concentrating mechanisms (CCM) augment the chemical conditions in the locality of the primary CO 2 -fixing enzyme (D-ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO)), resulting in increased photosynthesis (Rae et al 2013). In Antarctic habitats such mechanisms are essential for nutrient input.…”

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

“…HCO 3 − transport is generally coupled to Na + gradients or ATP hydrolysis and facilitated uptake is hypothesized to couple oxidation of NAD(P)H to unidirectional hydration of CO 2 ( Fig. 1) (8). Accumulation of charged HCO 3 − is preferable to accumulation of CO 2 because HCO 3 − escapes much less readily through the cell membrane, as we discuss below.…”

“…Perturbations to either component disrupt the CCM and produce mutants that require elevated CO 2 for growth (9,10). Two energetically activated transport mechanisms-HCO 3 − transport and facilitated uptake of CO 2 -enable accumulation of bicarbonate (HCO 3 − ) in the cytosol (8). HCO 3 − transport is generally coupled to Na + gradients or ATP hydrolysis and facilitated uptake is hypothesized to couple oxidation of NAD(P)H to unidirectional hydration of CO 2 ( Fig.…”

“…1) wherein the CCM has two primary components: active accumulation of inorganic carbon (Ci) in the cytosol and organization of RuBisCO with carbonic anhydrase (CA) inside proteinaceous organelles called carboxysomes (8). Perturbations to either component disrupt the CCM and produce mutants that require elevated CO 2 for growth (9,10).…”