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The giant clam photosymbiosis is a physically optimized photoconversion system for the most intense sunlight on Earth

Citation

Holt, Amanda; Sweeney, Alison; Rehm, Lincoln (2022), The giant clam photosymbiosis is a physically optimized photoconversion system for the most intense sunlight on Earth, Dryad, Dataset, https://doi.org/10.5061/dryad.xsj3tx9k4

Abstract

Giant clams are photosymbiotic with unicellular algae ("zooxanthellae") organized in the clam's mantle tissue. This tissue has an especially low albedo for a photosynthetic system, generally less than 10\% at all visible wavelengths. This efficient absorbance of light occurs in the ecological context of the high solar irradiances in intertidal habitats near the equator. At these light levels, photosynthetic systems typically adapt to absorb less light in order to prevent radiative damage to chloroplasts. Giant clams are therefore unusual.  If the giant clam photosymbiosis proves to be simultaneously efficient at absorption and at phototransduction at these irradiances, they are potentially remarkably productive and an important source of bioinspiration. We showed previously that the clams organize algae into vertical pillars in the mantle tissue. The clams' iridocytes, or optically structured skin cells on the surface of the tissue, then function to evenly distribute incoming solar irradiance along the vertical faces of the pillars. The result is that zooxanthellae in the system absorb solar power at lower rates than that of incoming solar flux. The overall energetic performance of this phtooconversion scheme has, however, been difficult to characterize given the complex three-dimensional structure and the fact that it is coupled to a much more voluminous, respiring animal. Here we use a combination of photochemical characterization and new quantitative modeling of data from the literature to estimate the photochemical efficiency as a function of incoming irradiance of the initial electron-transfer events. Our approach is to consider the clam mantle tissue in isolation as a meta-material for photoconversion. To do this, we developed a method to directly measure the system's photochemical efficiency with spatial resolution of 10's of microns using optical microprobes threaded through the tissue. These experimental efficiency data then serve as ground-truthing for a subsequent reanalysis of photosynthesis-irradiance curves of clams taken from the literature. For this quantitative re-analysis, we incorporated the clam system's quantum efficiency as a function of irradiance per cell into a Monte Carlo model of radiative transfer among cells to find the tissue's area-specific oxygen evolution apart from any sinks. We found that cells located within the dense clam system had fluorescence transients (i.e., Kautsky curves), a direct measure of the efficiency of PS II) that were very slow and of low intensity, particularly for a dense system, consistent with photochemical efficiencies generally greater than 50\% and often greater than 90\%. When incorporated into a larger computational model, we found that mature Tridacnid clams can efficiently perform photoconversion of light energy into chemical energy at light intensities many times more intense than the maximum time-averaged environmental radiance, or even the solar constant. The intensities to which the clam is adapted, however, can be found in strong wave-lensed pulses of irradiance that are characteristic of the clams' habitats. This surprising result makes sense if the system has evolved to both avoid damage from and utilize the power in the intense pulses of light that result from wave-lensing. Our model predicts that by evolving to compensate for the intense pulses of solar energy produced by wave-lensing, the clam system can perform photochemical conversion of radiation at intensities many times greater than the solar constant at around 90\% quantum efficiency. This result in turn suggests a strategy for organic, engineered materials performing photoconversion under solar concentration.

Methods

Data for fluorescence was collected using a photomultiplier tube and an oscilliscope. The turn-on point was determined for each dataset by hand. This data is stored in folders organized by date and processed using a MATLAB program to a table of numbers representing values used to calculate the photosynthetic quantum efficiencies for each sample. Data for absorption was collected using a spectrometer. The transmission, reflection and blank data were recorded on the spectrometer and stored in folders organized by date. This data was processed using MATLAB to calculate the absorption for each set of reflection and transmission data. Three-dimensional models for clam tissue were generated using a MATLAB program. The Monte Carlo simulation was run on a university GPU with code written in C++ and CUDA. Data from the Monte Carlo simulation was transferred to a local computer and analyzed using a program written in MATLAB. The productivity for each three-dimensional model was calculated using a program written in MATLAB. The photosynthetic efficiencies used in the productivity code resulted from fitting using MATLAB. 

Usage Notes

MATLAB or open source: Octave or Python (NumPy), C++ and CUDA, and Avantes spectrometer sofware (or whatever software one's USB spectrometer uses)

Funding

National Science Foundation