Physiological aspects of CO2 and HCO3− transport by cyanobacteria: a review

1990 ◽  
Vol 68 (6) ◽  
pp. 1291-1302 ◽  
Author(s):  
Anthony G. Miller ◽  
George S. Espie ◽  
David T. Canvin

Cyanobacteria grown at air levels of CO2, or lower, have a very high photosynthetic affinity for CO2. For ceils grown in carbon-limited chemostats at pH 9.6, the K0.5 (CO2) for whole cell CO2 fixation is about 3 nM. This is in spite of a K0.5 (CO2) for cyanobacterial ribulose bisphosphate carboxylase/oxygenase of about 200 μM. It is now clear that cyanobacteria can photosynthesize at very low CO2 concentrations because they raise the CO2 concentration dramatically around the carboxylase. This rise in the intracellular CO2 concentration involves the active transport of HCO3− and CO2, perhaps by separate transport systems. The transport of HCO3− often requires millimolar levels of Na+, and this provides a ready means of initiating HCO3− transport. The active transport of CO2 requires only micromolar levels of Na+. In the rather dense cell suspensions used in transport studies the extent of CO2 uptake is often limited by the rate at which CO2 can be formed from the HCO3− in the medium. The addition of carbonic anhydrase relieves this kinetic limitation on CO2 transport. The active transport of CO2 can be selectively inhibited by the structural analog carbon oxysulfide (COS). When HCO3− transport is allowed in the presence of COS there is a substantial net leakage of CO2 from the cells. This leaked CO2 results from the intracellular dehydration of the accumulated HCO3−. This CO2 is normally scavenged by the active CO2 pump. If cells are allowed to transport H13C18O18O18O− for 5 s and if CO2 transport is suddenly quenched by the addition of COS, then a rapid leakage of 13C16O16O occurs. If the rapidly released CO2 was actually present in the cells before the addition of the COS, then the intracellular CO2 concentration would have been about 0.6 mM. Not only is this a high concentration, but since the leaked CO2 was completely depleted of the initial 18O, it must have been in rapid equilibrium with the total dissolved inorganic carbon within the cells. Cells grown on high levels of inorganic carbon, either as CO2 or HCO3−, lack the active HCO3− system but still retain a capacity, albeit reduced, for CO2 transport. Cyanobacteria seem to adjust their complement of inorganic carbon transport systems so that the K0.5 for transport is close to the inorganic carbon concentration of the growth medium.

1998 ◽  
Vol 76 (6) ◽  
pp. 1072-1083 ◽  
Author(s):  
Yusuke Matsuda ◽  
Gale G Bozzo ◽  
Brian Colman

The regulation of the expression of the inorganic carbon concentrating mechanism (CCM) in aquatic photoautotrophs, particularly green algae, has been thought to require light and active photosynthesis. Recent studies, however, have indicated that there may be a light-independent pathway of signal transduction in green algae that may regulate the expression of CCMs in response to changes in ambient dissolved inorganic carbon (DIC) concentration. In the green alga, Chlorella ellipsoidea, changes in the rate of transport of both CO2 and HCO3- were shown to occur in response to the CO2 concentration in the bulk medium, independent of pH, whereas other inorganic carbon species, which might induce or repress DIC transport expression, were shown to change markedly with the pH of the medium. Furthermore, neither changes in the CO2 concentration around ribulose bisphosphate carboxylase-oxygenase (Rubisco) nor light were shown to be critical factors in regulating CCM expression in this alga. CO2-insensitive mutants of Chlorella ellipsoidea were recently isolated in which DIC transport operates constitutively at maximum activity. These results strongly suggest that a direct CO2 sensing mechanism may operate at the cell surface in Chlorella ellipsoidea and that this mechanism may trigger the repression of the expression of DIC transport in response to high CO2. Some supportive evidence for this hypothesis has also been obtained in other green algae, Chlamydomonas reinhardtii and Chlorella kessleri. The possibility of the occurrence of a direct sensing mechanism for CO2, its implications, and possible coexistence of other regulatory systems for CCM expression are discussed.Key words: green algae, Chlorella, signal transduction, CO2-insensitive mutants, CO2-sensing mechanism.


2016 ◽  
Vol 113 (36) ◽  
pp. E5354-E5362 ◽  
Author(s):  
Niall M. Mangan ◽  
Avi Flamholz ◽  
Rachel D. Hood ◽  
Ron Milo ◽  
David F. Savage

Many carbon-fixing bacteria rely on a CO2 concentrating mechanism (CCM) to elevate the CO2 concentration around the carboxylating enzyme ribulose bisphosphate carboxylase/oxygenase (RuBisCO). The CCM is postulated to simultaneously enhance the rate of carboxylation and minimize oxygenation, a competitive reaction with O2 also catalyzed by RuBisCO. To achieve this effect, the CCM combines two features: active transport of inorganic carbon into the cell and colocalization of carbonic anhydrase and RuBisCO inside proteinaceous microcompartments called carboxysomes. Understanding the significance of the various CCM components requires reconciling biochemical intuition with a quantitative description of the system. To this end, we have developed a mathematical model of the CCM to analyze its energetic costs and the inherent intertwining of physiology and pH. We find that intracellular pH greatly affects the cost of inorganic carbon accumulation. At low pH the inorganic carbon pool contains more of the highly cell-permeable H2CO3, necessitating a substantial expenditure of energy on transport to maintain internal inorganic carbon levels. An intracellular pH ≈8 reduces leakage, making the CCM significantly more energetically efficient. This pH prediction coincides well with our measurement of intracellular pH in a model cyanobacterium. We also demonstrate that CO2 retention in the carboxysome is necessary, whereas selective uptake of HCO3− into the carboxysome would not appreciably enhance energetic efficiency. Altogether, integration of pH produces a model that is quantitatively consistent with cyanobacterial physiology, emphasizing that pH cannot be neglected when describing biological systems interacting with inorganic carbon pools.


1998 ◽  
Vol 76 (6) ◽  
pp. 1010-1017 ◽  
Author(s):  
John Beardall ◽  
Andrew Johnston ◽  
John Raven

Most microalgae possess a mechanism for actively transporting inorganic carbon that concentrates CO2 at the active site of the carbon fixing enzyme ribulose bisphosphate carboxylase-oxygenase (Rubisco). This review considers the effects of environmental factors on the capacity and activity of microalgal CO2-concentrating mechanisms. Limitation of energy supply by light availability decreases the rate of inorganic carbon transport and cells grown under light-limited conditions have a reduced capacity for CO2 accumulation. Phosphorus limitation also reduces the capacity of algal cells to accumulate CO2, whereas both the rate of supply of nitrogen and the form in which it is made available interact in various complex ways with carbon utilization. The potential role of other nutrients in modulating inorganic carbon transport is also discussed. The capacity of algae for carbon accumulation is also affected by CO2 supply, which, in turn, is a function of the interactions between ionic strength of the growth medium, pH, cell density in culture, aeration rate, and inorganic carbon concentration in the medium. The effects of these interacting parameters are discussed, together with an assessment of the possible roles and significance of CO2-concentrating mechanisms to microalgae in marine and freshwater ecosystems.Key words: carbon acquisition, microalgae, CO2-concentrating mechanism, light, nutrient limitation, CO2 supply.


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