Environmental regulation of CO2-concentrating mechanisms in microalgae

1998 ◽  
Vol 76 (6) ◽  
pp. 1010-1017 ◽  
Author(s):  
John Beardall ◽  
Andrew Johnston ◽  
John Raven
Keyword(s):  
Inorganic Carbon ◽  
Light Availability ◽  
Phosphorus Limitation ◽  
Aeration Rate ◽  
Carbon Accumulation ◽  
Ribulose Bisphosphate Carboxylase ◽  
Carbon Utilization ◽  
Bisphosphate Carboxylase ◽  
Inorganic Carbon Transport ◽  
Carbon Transport

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.

scholarly journals pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism

2016 ◽  
Vol 113 (36) ◽  
pp. E5354-E5362 ◽  
Author(s):  
Niall M. Mangan ◽  
Avi Flamholz ◽  
Rachel D. Hood ◽  
Ron Milo ◽  
David F. Savage
Keyword(s):  
Intracellular Ph ◽  
Inorganic Carbon ◽  
Quantitative Description ◽  
Carbon Accumulation ◽  
Energetic Efficiency ◽  
Ribulose Bisphosphate Carboxylase ◽  
Competitive Reaction ◽  
Bisphosphate Carboxylase ◽  
Concentrating Mechanism ◽  
Ribulose Bisphosphate Carboxylase Oxygenase

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.

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
Keyword(s):  
Active Transport ◽  
Inorganic Carbon ◽  
Dissolved Inorganic Carbon ◽  
Structural Analog ◽  
Transport Systems ◽  
Ribulose Bisphosphate Carboxylase ◽  
High Concentration ◽  
Bisphosphate Carboxylase ◽  
Ribulose Bisphosphate Carboxylase Oxygenase ◽  
Inorganic Carbon Transport

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.

Inorganic carbon transport in some marine microalgal species

1991 ◽  
Vol 69 (5) ◽  
pp. 1032-1039 ◽  
Author(s):  
M. J. Merrett
Keyword(s):  
Carbonic Anhydrase ◽  
Inorganic Carbon ◽  
Silicone Oil ◽  
Ph Regulation ◽  
Carbonic Anhydrase Activity ◽  
Carbon Accumulation ◽  
Bicarbonate Transport ◽  
High Affinity ◽  
Inorganic Carbon Transport ◽  
Carbon Transport

Inorganic carbon transport was investigated in a range of marine microalgae. A small-celled strain of Stichococcus bacillaris, containing appreciable carbonic anhydrase activity, showed a high affinity for CO2, while measurement of the internal inorganic carbon pool by the silicone oil layer centrifugal filtering technique showed cells concentrated inorganic carbon up to 20-fold in relation to the external medium at pH 5.0 but not pH 8.3. The addition of 14CO2 or H14CO3− to cells in short-term kinetic experiments at pH 8.3 confirmed that only CO2 provides the exogenous substrate for substantial inorganic carbon accumulation within the cell. High-affinity HCO3− transport in Phaeodactylum tricornutum and Porphyridium purpureum is dependent on sodium ions, while intracellular carbonic anhydrase increased the steady-state flux of CO2 from inside the plasmalemma to Rubisco. In the presence of HCO3− the intracellular pH in cells of P. purpureum is 7.1 but on carbon starvation the pH falls to 6.0. Ethoxyzolamide blocks bicarbonate-dependent alkalinization of the cytosol, confirming a central role for carbonic anhydrase–bicarbonate in cytosolic pH regulation. Carbonic anhydrase activity is pH dependent in P. purpureum so synergistic interaction between CO2 uptake and bicarbonate transport may occur.

Regulation of dissolved inorganic carbon transport in green algae

1998 ◽  
Vol 76 (6) ◽  
pp. 1072-1083 ◽  
Author(s):  
Yusuke Matsuda ◽  
Gale G. Bozzo ◽  
Brian Colman
Keyword(s):  
Green Algae ◽  
Inorganic Carbon ◽  
Dissolved Inorganic Carbon ◽  
Inorganic Carbon Transport ◽  
Carbon Transport

Analysis of high CO2 requiring mutants indicates a central role for the 5′ flanking region of rbc and for the carboxysomes in cyanobacterial photosynthesis

1990 ◽  
Vol 68 (6) ◽  
pp. 1303-1310 ◽  
Author(s):  
Aaron Kaplan
Keyword(s):  
Inorganic Carbon ◽  
Quantitative Model ◽  
Photosynthetic Performance ◽  
Kanamycin Resistance ◽  
Open Reading Frames ◽  
Bisphosphate Carboxylase ◽  
Insertional Inactivation ◽  
Flanking Region ◽  
Inorganic Carbon Transport ◽  
Reading Frames

The mutants E1 and O221, isolated from Synechococcus sp. PCC7942, exhibit a very low apparent photosynthetic affinity for both extracellular and intracellular inorganic carbon and hence require high CO2 concentrations for growth. These mutants possess defective carboxysomes, but the activity of ribulose 1,5-bisphosphate carboxylase is normal. The mutations in these mutants have been mapped to the 5′-flanking region of rbc, and two open reading frames, the functions of which are not yet known, have been identified in this region. Insertional inactivation (by inserting a kanamycin-resistance cartridge) of one of these open reading frames, where the mutation in O221 is located, resulted in a new high CO2 requiring phenotype. This mutant contains defective carboxysomes similar to those of O221. The role of the rbc and its 5′-flanking region in the photosynthetic performance of cyanobacteria and the structural organization of the carboxysomes are discussed in view of our recently proposed quantitative model for inorganic carbon transport and photosynthesis in cyanobacteria.

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