Despite living in oligotrophic tropical waters, giant clams can grow to large sizes because they live in symbiosis with extracellular phototrophic dinoflagellates (zooxanthellae) and receive photosynthates from them. The physical presence of zooxanthellae in five organs (colorful outer mantle, whitish inner mantle, ctenidium, hepatopancreas and foot muscle) of Tridacna squamosa had been confirmed by microscopy, and high densities of zooxanthellae were detected in specific regions of the inner mantle and foot muscle. Symbiotic dinoflagellates use form II ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) to fix inorganic carbon during C3 photosynthesis. Using qPCR primers that were designed comprehensively against all known zooxanthellal form II RuBisCO gene sequences (rbcII) in existing databases, we demonstrated that the outer mantle of T. squamosa (TS) had the greatest phototrophic potential as reflected by its high zooxanthellal rbcII (TSZrbcII) transcript level, which varied among different regions of the outer mantle. The other four organs also expressed moderate levels of TSZrbcII, despite the lack of iridophores and direct light exposure. Importantly, light exposure led to significant increases in the protein abundance of TSZRBCII in the outer mantle but not the other four organs. Taken together, these results indicate that organs inside the mantle cavity had low phototrophic potentials, but zooxanthellae residing inside these organs might serve some unidentified functions to benefit the host.