In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis

The photosynthesis-irradiance (PE) relationship links indices of phytoplankton biomass (e.g. chl) to rates of primary production. The PE curve can be characterized by two variables: the light-limited slope (alpha(b)) and the light-saturated rate (P-max(b)) of photosynthesis. Variability in PE curves can be separated into two categories: that associated with changes in the light saturation index, E-k (=P-max(b)/alpha(b)) and that associated with parallel changes in alpha(b)and P-max(b) (i.e. no change in E-k). The former group we refer to as "E-k-dependent" variability, and it results predominantly from photoacclimation (i.e. physiological adjustments in response to changing light). The latter group we refer to as "E-k-independent" variability, and its physiological basis is unknown. Here, we provide the first review of the sporadic field and laboratory reports of E-k-independent variability, and then from a stepwise analysis of potential mechanisms we propose that this important yet largely neglected phenomenon results from growth rate-dependent variability in the metabolic processing of photosynthetically generated reductants (and generally not from changes in the oxygen-evolving PSII complexes). Specifically, we suggest that as growth rates decrease (e.g. due to nutrient stress), reductants are increasingly used for simple ATP generation through a fast (<1s) respiratory pathway that skips the carbon reduction cycle altogether and is undetected by standard PE methodologies. The proposed mechanism is consistent with the field and laboratory data and involves a simple new "twist" on established metabolic pathways. Our conclusions emphasize that simple reductants, not reduced carbon compounds, are the central currency of photoautotrophs.