Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway

SUMMARY Iron is involved in many photosynthetic, respiratory and nitrogen assimilation reactions of plants as Fe bound tightly to polypeptides catalysing redox reactions. Manganese is involved as tightly bound Mn in photoreaction II of photosynthesis and in certain superoxide dismutases, while loosely bound Mn2+ is the unique activator of some enzymes, and is an alternative to Mg2+ in activating many enzymes. This paper uses data on the quantitative role of Fe and Mn in catalysts to predict the efficiency with which Fe and Mn are used in C assimilation [mol C assimilated (mol catalytic metal in enzyme)−1 s−1] and the metal cost of C assimilation [mol catalytic metal in enzyme (mol C assimilated)−1 s−1] in photolithotrophic growth in relation to genetic and environmental variables. The genetic variables were the relative content of thylakoid proteins in major taxa (cyanobacteria and red algae, chlorophytes and chromophytes) and smaller-scale taxonomic differences (various subtypes of C4 metabolism, and C3 metabolism, in terrestrial vascular plants). The environmental variables were the range of photon flux densities in which photolithotrophic growth of O2 evolvers can occur, and the inorganic C supply conditions controlling the repression/de-repression of the inorganic C concentrating mechanism in cyanobacteria and microalgae. The results of the computations yield the following conclusions. The largest predicted difference in Fe and Mn costs of photolithotrophic growth is related to changes in the photon flux density for growth. The predicted Fe cost increased 50-fold, and the Mn cost increased 80-fold, at the lowest extreme of photon flux density compared to the highest found naturally. The increase is partly countered by the larger ratio of light-harvesting pigments to thylakoid protein complexes assumed for the cells grown at low photon flux densities, although the extent of the increase in photosynthetic unit size is limited by considerations of efficiency of excitation energy transfer. However, the major influences are the higher pigment content in biomass enabling a larger fraction of incident light to the absorbed, and the sub-maximal specific reaction rates of redox catalysts (whose content is constrained via excitation energy transfer considerations) at very low photon flux densities. A smaller difference, four-fold or less, in Fe and Mn costs of photolithotrophic growth, is predicted by comparing major taxa (cyanobacteria plus red algae; chlorophytes plus chromophytes) with contrasting ratios of thylakoid redox catalysts. Differences in Fe and Mn costs of growth of less than two-fold are predicted when the Fe- and Mn-efficient organisms with CO2− concentrating mechanisms (C4 land plants; algae with active inorganic C influx) and high requirements for ATP relative to NADPH, are compared with organisms relying on CO2 diffusion from air or air-equilibrated solutions and C3 biochemistry. These predictions of variations in Fe and Mn costs of photolithotrophy have implications for the ecology of phototrophs.