DOI: 10.5061/dryad.xsj3tx9k4
title: The giant clam photosymbiosis is a physically optimized photoconversion system for the most intense sunlight on Earth

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