Dynamics of nitrogen reserves in the form of guanine crystals as an adaptation of Amphidinium carterae for various illumination levels
Abstract
It is known that biogenic guanine crystals are widely used by animals to manipulate light. Due to their high refraction index and plate-like arrangement, guanine crystal arrays can serve as diffuse scatterers, broad- and narrowband reflectors, tunable photonic crystals, and image-forming mirrors.
Recently, crystalline inclusions composed of guanine or related purines have also been identified in various phylogenetically unrelated photosynthetic microalgae. In dinoflagellate Amphidinium carterae, guanine crystals were found to serve as a long-term, high-capacity store of nitrogen.
However, their role in light manipulation in unicellular photosynthetic eukaryotes has also been speculated previously. Using confocal Raman microscopy, we have visualized crystalline guanine within intact A. carterae cells cultivated under various nutritional and light conditions and found that the location of guanine crystals can depend on the intensity of illumination.
We have found that the usual site of the guanine de novo biosynthesis and formation of guanine crystals is at the cell periphery, between the cell wall and the plastids, regardless of the actual illumination level. Even being cultivated in total darkness for several weeks or months, after supplementing the medium with a nitrogen source, the cells are forming and storing guanine crystals at the periphery.
However, depending on the illumination stress levels, the position of guanine crystals may be changed. When the cells are cultivated under a continuous supply of inorganic nitrogen sources but exposed to very low light intensity, their adaptation consists of an increase in the amount of plastids and deposition of the guanine crystals behind the plastids, closer to the center of the cell.
Acting as photonic mirrors or diffusers for redirecting untrapped photons back to plastids, guanine crystals might increase the efficiency of photosynthesis. In the case of cultivation at a high light intensity, extensive layers of guanine crystals are organized at the periphery, shielding plastids from excessive illumination.
This suggests that guanine crystals at least in A. carterae can play a certain role in regulating photosynthetic efficiency and by default protecting plastids from photodamage.