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 $\mathrm{O}$${}_2$, 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.

• Received 13 June 2023
• Revised 1 May 2024
• Accepted 6 May 2024

DOI:https://doi.org/10.1103/PRXEnergy.3.023014

Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

Published by the American Physical Society