The Giant Clam Photosymbiosis is a Physically Optimal Photoconversion System for the Most Intense Sunlight on Earth

Abstract

Giant clams are photosymbiotic with unicellular algae ("zooxanthellae") organized in the clams 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 systems photochemical efficiency with spatial resolution of 10s 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 systems quantum efficiency as a function of irradiance per cell into a Monte Carlo model of radiative transfer among cells to find the tissues 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 1), 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 suggest a strategy for engineered organic and biological composite materials performing photoconversion under solar concentration. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/530416v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@52764borg.highwire.dtl.DTLVardef@1d453d6org.highwire.dtl.DTLVardef@cc461dorg.highwire.dtl.DTLVardef@10f32f2_HPS_FORMAT_FIGEXP M_FIG C_FIG