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Mangan, Niall M; Flamholz, Avi; Hood, Rachel D; Milo, Ron; Savage, David F
Proceedings of the National Academy of Sciences - PNAS, 09/2016, Volume: 113, Issue: 36Journal Article
Many carbon-fixing bacteria rely on a CO sub(2) concentrating mechanism (CCM) to elevate the CO sub(2) 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 O sub(2) 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 H sub(2)CO sub( 3), necessitating a substantial expenditure of energy on transport to maintain internal inorganic carbon levels. An intracellular pH approximately 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 CO sub(2) retention in the carboxysome is necessary, whereas selective uptake of HCO sub(3)- 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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