The multiplicity of roles for (bi)carbonate in photosystem II operation in the hypercarbonate-requiring cyanobacterium Arthrospira maxima

Abstract

Arthrospira maxima is unique among cyanobacteria, growing at alkaline pH (<11) in concentrated (bi)carbonate (1.2 M saturated) and lacking carbonic anhydrases. We investigated dissolved inorganic carbon (DIC) roles within PSII of A. maxima cells oximetrically and fluorometrically, monitoring the light reactions on the donor and acceptor sides of PSII. We developed new methods for removing DIC based on a (bi)carbonate chelator and magnesium for (bi)carbonate ionpairing. We established relative affinities of three sites: the water-oxidizing complex (WOC), non-heme iron/QA–, and solvent-accessible arginines throughout PSII. Full reversibility is achieved but (bi)carbonate uptake requires light. DIC depletion at the non-heme iron site and solvent-accessible arginines greatly reduces the yield of O2 due to O2 uptake, but accelerates the PSII–WOC cycle, specifically the S2→S3 and S3→S0 transitions. DIC removal from the WOC site abolishes water oxidation and appears to influence free energy stabilization of the WOC from a site between CP43-R357 and Ca2+.