Regulation of cyanobacterial CO2-concentrating mechanisms through transcriptional induction of high-affinity Ci-transport systems

Abstract

Approximately 50% of global CO2-based productivity is now attributed to the activity of phytoplankton, including ocean-dwelling cyanobacteria. In response to inherent restrictions on the rate of CO 2 supply in the aquatic environment, cyanobacteria have evolved a very efficient means of capturing inorganic carbon (Ci), as either CO2 or HCO3- for photosynthetic carbon fixation. This capturing mechanism, known as a CO2-concentrating mechanism (CCM), involves the operation of active CO2 and HCO 3- transporters and results in the concentration of CO2 around RuBisCO, in a unique microcompartment called the carboxysome. The CCM exhibits two basic physiological states: a constitutive, low-affinity state; and a high-affinity state, which is induced in response to Ci limitation. Many of the genetic components of the CCM, including genes encoding Ci transporters, have been identified. It is apparent that the expression of genes encoding the inducible, high-affinity Ci transporters is particularly sensitive to Ci availability, and we are now interested in defining how cyanobacterial cells sense and respond to Ci limitation at the transcriptional level. Current theories include direct sensing of external Ci; sensing of internal Ci-pool fluctuations; and detection of changes in photorespiratory intermediates, carbon metabolites, or redox potential. At present, there is no consensual view. We have investigated the physiological and transcriptional responses of CCM mutants and wildtype strains to pharmacological treatments and various light, O2, and Ci regimes. Our data suggest that perception of Ci limitation by a cyanobacterial cell is either directly or indirectly related to the size of the internal Ci pool within the cell, in an oxygen-dependent manner.