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Keywords:

  • algae;
  • CO2-concentrating mechanism, carbonic anhydrase;
  • proton pump;
  • pyrenoid;
  • stroma;
  • thylakoid;
  • thylakoid lumen

ABSTRACT

A testable mechanism of CO2 accumulation in photolithotrophs, originally suggested by Pronina & Semenenko, is quantitatively analysed. The mechanism involves (as does the most widely accepted hypothesis) the delivery of HCO3 to the compartment containing Rubisco. It differs in proposing subsequent HCO3 entry (by passive uniport) to the thylakoid lumen, followed by carbonic anhydrase activity in the lumen; uncatalysed conversion of HCO3 to CO2, even at the low pH of the lumen, is at least 300 times too slow to account for the rate of inorganic C acquisition. Carbonic anhydrase converts the HCO3 to CO2 at the lower pH maintained in the illuminated thylakoid lumen by the light-driven H+ pump, generating CO2 at 10 times or more the thylakoid HCO3 concentration. Efflux of this CO2 can suppress Rubisco oxygenase activity and stimulate carboxylase activity in the stroma. This mechanism differs from the widely accepted hypotheses in the required location of carbonic anhydrase, i.e. in the thylakoid lumen rather than the stroma or pyrenoid, and in the need for HCO3 influx to thylakoids. The capacity for anion (assayed as Cl) entry by passive uniport reported for thylakoid membranes is adequate for the proposed mechanism; if the Cl channel does not transport HCO3, HCO3 entry could be by combination of the Cl channel with a Cl HCO3 antiporter. This mechanism is particularly appropriate for organisms which lack overt accumulation of total inorganic C in cells, but which nevertheless have the gas exchange characteristics of an organism with a CO2-concentrating mechanism.