Simple Mechanism for Optimal Light-Use Efficiency of Photosynthesis Inspired by Giant Clams

Abstract

In photosymbiotic giant clams, vertical columns of single-celled algae absorb sunlight that has first been forward scattered from a superficial layer of light-scattering cells called iridocytes. In principle, this arrangement could lead to a highly efficient system but it has been unclear how to calculate a productivity denominator to normalize the performance of the system. Inspired by the geometry observed in the clam, we have created an analytical model that calculates the idealized performance of a system with a geometry similar to the clam. In our model, photosynthesis-irradiance behavior obeys that of algal cells isolated from clams. Using a standard rate of eight photons of photosynthetically active radiation required to create one molecule of O2, we find that a fixed geometry of the “light-dilution” strategy employed by the clams can reach a quantum efficiency of 43% relative to the solar resource in intense tropical sunlight. In comparing the performance of the model to published photosynthesis-irradiance relations of living clams, we have observed that the living system easily exceeds the performance of the static model. Therefore, we have next considered a model in which the system geometry changes dynamically to optimize the quantum efficiency as a function of the solar irradiance. In this scenario, with changes in irradiance typical of a sunny tropical day, the performance of the model was consistent with that of large mature living clams and had a quantum efficiency of 67%. We also show that a similar dynamic modulation of the clam-tissue geometry could plausibly occur in the living animals. We have considered the possibility that efficiency gains in the living system could also occur via further optimization of per-cell absorbance of multiply scattered light within the highly absorbing system. However, a numerical model of radiative transfer within clam tissue that captures realistic multiple scattering has not located efficiency gains relative to the simpler single-pass analytical model. Therefore, we infer that additional resource efficiency over the dynamic, large-clam-like model would require nontrivial organization among cells at small length scales. We also observe that boreal spruce forests coupled to atmospheric haze may realize the same scale-invariant scattering-and-absorbance strategy as the clams but at a different, larger, length scale. Given these results, our model may demonstrate the maximum realizable light-use efficiency of a large photosynthetic system relative to the solar resource. The general principles here also readily generalize to any photosynthetic cell type or organic photoconversion material and solar-irradiance regime. They could therefore provide inspiration both for engineering novel efficient photoconversion processes and materials and inform optimal land-use estimates for efficient industrial biomass production. Published by the American Physical Society 2024