Topic 8.1 CO2 Pumps

Oxygenic photosynthesis invariably utilizes rubisco as the core enzyme involved in the incorporation of inorganic carbon into the skeletons of organic compounds. However,

  1. the present concentration of atmospheric CO2 does not saturate the carboxylase activity, and
  2. an oxygenase activity competitive with the carboxylase activity is an intrinsic function of the enzyme.

These features can help us to visualize why many O2-producing organisms contain concentrating mechanisms for the fixation of inorganic carbon. These mechanisms actively transport HCO3, CO2, and/or H+ to increase the concentration of CO2, and the CO2/O2 ratio, at the active site of rubisco, thereby favoring carboxylase activity. In most land plants, the CO2-concentrating mechanisms are C4 photosynthesis and crassulacean acid metabolism (CAM). While present in aquatic plants, CO2 and HCO3 pumps at the plasma membrane have been studied most extensively in prokaryotic cyanobacteria and eukaryotic algae.

In response to changing concentrations of inorganic carbon in aqueous environments, many photosynthetic organisms induce mechanisms for concentrating CO2 and thus favor the carboxylation reaction of rubisco (Ogawa and Kaplan 1987; Giordano et al. 2005). Although cyanobacteria and algae exhibit symptoms of photorespiration (retarded growth, precocious senescence) when the air used to aerate their medium is switched from 5% CO2 to 0.03% CO2, these organisms rapidly develop the ability to concentrate inorganic carbon so that they no longer photorespire. In cyanobacteria, two cellular assemblies are essential for the concentration of inorganic carbon:

  1. transporters located at both the plasma and the thylakoid membranes, and
  2. carboxysomes, where most of the rubisco and the carbonic anhydrase reside.

Web Figure 8.1.A   The cyanobacterial CO2 concentrating mechanism. Translocators located in the plasma membrane (purple box) and the thylakoid membrane (blue box) pump HCO3 and CO2 into the cytosol and thylakoid of a cyanobacterium. The diffusional resistance to efflux and the internal gradient of HCO3 drive the inorganic carbon to the carboxysome. The carboxysomal carbonic anhydrase catalyzes the interconversion of HCO3 and CO2 and, in so doing, increases the concentration of CO2 around rubisco, facilitating the carboxylation of ribulose 1,5-bisphosphate.

The carboxysome is a unique microbody surrounded by a protein coat that contains most of the cellular rubisco and is distinct from the thylakoid membranes. At low levels of atmospheric CO2, cyanobacteria accumulate inorganic carbon in the cytosol using HCO3 and CO2 pumps associated with plasma and thylakoid membranes, respectively. The HCO3 diffuses from the cytosol into the carboxysome and, once inside the compartment, a carbonic anhydrase converts HCO3 to CO2 for the rubisco reaction.

In short, the flow of inorganic carbon from the environment to the close proximity of rubisco requires: (1) the accumulation of HCO3 in the cytosol; (2) its transport to the rubisco-containing carboxysomes; and (3) the conversion HCO3 to CO2 by carboxysomal carbonic anhydrase (Badger and Price 2003). The concerted enrichment of CO2 around rubisco ultimately suppresses the oxygenation of ribulose 1,5-bisphosphate and, in so doing, eliminates the need for photorespiration.