The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances

Cyanobacteria (blue-green algae) possess an environmental adaptation for survival at low CO2 concentrations. The adaptation is known as a CO2 concentrating mechanism (CCM), and it functions to actively transport and accumulate inorganic carbon ( and CO2; Ci) within the cell and then uses this Ci pool to provide elevated CO2 concentrations around the primary CO2-fixing enzyme, ribulose bisphosphate carboxylase-oxygenase (Rubisco). It appears that the site of CO2 elevation is within a unique microcompartment known as the carboxysome, which is a proteinaceous polyhedral body that contains most, if not all, of the Rubisco within the cell. This review covers comparative aspects of physiology, genetics, and proteins involved in the cyanobacterial CCM with particular focus on recent advances. This review highlights information on three strains of unicellular cyanobacteria, namely Synechocystis PCC6803 (freshwater strain; for which a full genome database is now available), Synechococcus PCC7002 (coastal marine strain) and Synechococcus PCC7942 (freshwater strain). Genes that may be involved in the CCM, directly or indirectly, are summarized in tabular form. For Synechocystis PCC6803, the number of genes related to CCM activity is now in excess of 50; however, 19 of these components have the potential to code for several distinct type-1, NADH dehydrogenase complexes.Key words: cyanobacteria, CO2 concentrating mechanism, carboxysomes, genes, photosynthesis, transporters.

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pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1525145113 ◽

2016 ◽

Vol 113 (36) ◽

pp. E5354-E5362 ◽

Cited By ~ 69

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.

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Thylakoid localized bestrophin-like proteins are essential for the CO2 concentrating mechanism of Chlamydomonas reinhardtii

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1909706116 ◽

2019 ◽

Vol 116 (34) ◽

pp. 16915-16920 ◽

Cited By ~ 17

Author(s):

Ananya Mukherjee ◽

Chun Sing Lau ◽

Charlotte E. Walker ◽

Ashwani K. Rai ◽

Camille I. Prejean ◽

...

Keyword(s):

Chlamydomonas Reinhardtii ◽

Thylakoid Membrane ◽

Normal Growth ◽

Chloroplast Envelope ◽

Ribulose Bisphosphate Carboxylase ◽

Bisphosphate Carboxylase ◽

Thylakoid Lumen ◽

Concentrating Mechanism ◽

Essential Components ◽

Ribulose Bisphosphate Carboxylase Oxygenase

The green alga Chlamydomonas reinhardtii possesses a CO2 concentrating mechanism (CCM) that helps in successful acclimation to low CO2 conditions. Current models of the CCM postulate that a series of ion transporters bring HCO3− from outside the cell to the thylakoid lumen, where the carbonic anhydrase 3 (CAH3) dehydrates accumulated HCO3− to CO2, raising the CO2 concentration for Ribulose bisphosphate carboxylase/oxygenase (Rubisco). Previously, HCO3− transporters have been identified at both the plasma membrane and the chloroplast envelope, but the transporter thought to be on the thylakoid membrane has not been identified. Three paralogous genes (BST1, BST2, and BST3) belonging to the bestrophin family have been found to be up-regulated in low CO2 conditions, and their expression is controlled by CIA5, a transcription factor that controls many CCM genes. YFP fusions demonstrate that all 3 proteins are located on the thylakoid membrane, and interactome studies indicate that they might associate with chloroplast CCM components. A single mutant defective in BST3 has near-normal growth on low CO2, indicating that the 3 bestrophin-like proteins may have redundant functions. Therefore, an RNA interference (RNAi) approach was adopted to reduce the expression of all 3 genes at once. RNAi mutants with reduced expression of BST1–3 were unable to grow at low CO2 concentrations, exhibited a reduced affinity to inorganic carbon (Ci) compared with the wild-type cells, and showed reduced Ci uptake. We propose that these bestrophin-like proteins are essential components of the CCM that deliver HCO3− accumulated in the chloroplast stroma to CAH3 inside the thylakoid lumen.

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