Dynamics of Fluxes Through Photosynthetic Complexes in Response to Changing Light and Inorganic Carbon Acclimation in Synechococcus elongatus

Abstract

Cyanobacteria acclimate to environmental inorganic carbon (C_i) concentrations through re-organisations of photosynthetic function and the induction of carbon concentrating mechanisms (CCMs), which alter and constrain their subsequent acclimation to changing light. We grew cells acclimated to high C_i (4 mM) or low C_i (0.02 mM), shifted them from 50 μmol m⁻² s⁻¹ to 500 μmol m⁻² s⁻¹, and quantified their photosynthetic performance in parallel with quantitation of allocations to key indicator macromolecules. Pigments cell⁻¹ declined, PsbA (PS II), AtpB (ATP Synthase), RbcL (Rubisco) and GlnA (Glutamine Synthetase) increased, and PsaC (PS I) remained stable through the light shift. The increase in these protein pools was slower and smaller in low C_i cells, but acted in both cell types to re-normalise the electron fluxes through the catalytic complexes back toward values before the light shift (for PsbA and GlnA) or even below the initial flux per complex (for RbcL). In contrast, an increased electron flux per PsaC was sustained for at least 6 h after the increase in light. Initially, high levels of PS II cell⁻¹ and PS II connectivity in high C_i cells caused a more rapid net photoinactivation of PS II in high C_i cells than in low C_i cells, depressing the rate of PS II-specific electron transport (PS II ETR) to levels similar to linear ETR (net O₂ evolution minus respiration). In low C_i cells, PS II ETR remained in excess of linear ETR and may have helped maintain CCM activity. The pool sizes of PsbA, AtpB and GlnA correlated with cellular growth rate, and changed at similar rates in high C_i and low C_i cells when expressed on a generational rather than chronological timescale, which has implications for differing ecology of high and low C_i cells under variable natural light.