PH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism

Niall M. Mangan, Avi Flamholz, Rachel D. Hood, Ron Milo, David F. Savage*

*Corresponding author for this work

Research output: Contribution to journalArticle

48 Scopus citations

Abstract

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 cellpermeable H2 CO3 , 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 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.

Original languageEnglish (US)
Pages (from-to)E5354-E5362
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number36
DOIs
StatePublished - Sep 6 2016

Keywords

  • Carbon fixation|rubisco
  • Cyanobacteria|inorganic carbon
  • Systems biology

ASJC Scopus subject areas

  • General

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