Microalgae harnessed for biosynthesis of molecular crystals

Dinoflagellates can rapidly accumulate many nitrogen heterocycles from aqueous solutions into nitrogen-storage crystals, revealing a general mechanism for their metabolism of dissolved organic nitrogen. The crystallization behavior can be manipulated to generate crystals with tailored morphologies and optical properties, including birefringent xanthine spherulites, and to harness microalgae as cellular factories for producing molecular crystals from aqueous solutions under ambient conditions.

Highly reflective biogenic crystals such as guanine have potential as biocompatible alternatives to toxic inorganic optical materials. Engineered microbial cells have been used widely to generate high-value metabolites, but the biosynthesis of functional crystalline materials has not been achieved.

In marine dinoflagellates, guanine crystals act as high-capacity nitrogen stores that are used to overcome periodic deficiencies in environmental nitrogen. When nitrogen-starved Amphidinium carterae cells were transferred to a culture medium containing dissolved guanine at about 40 μM as the sole nitrogen source, guanine was depleted rapidly from the medium, concomitantly with the appearance of birefringent, polycrystalline spheroids composed of the β polymorph of guanine. These polycrystalline spheroids are housed in centrally located, membrane-bound vacuoles.

The vacuoles begin to accumulate crystals just 1–10 min after exposure to exogenous guanine, are fully formed after about 1–5 h and begin to disintegrate after 12–48 h. Dinoflagellates can directly uptake, crystallize and proliferate on numerous nitrogen heterocycles, suggesting that the storage of organic nitrogen in crystals and the subsequent release of organic nitrogen from these crystals is a general strategy for their metabolism of dissolved organic nitrogen.

Nitrogen heterocycles such as guanine are principal constituents of low molecular weight dissolved organic nitrogen, an abundant and persistent form of marine reduced nitrogen. Anthropogenic influences have led to increases in dissolved organic nitrogen, and rationalizing how microalgae metabolize nitrogen heterocycles is crucial to understanding dissolved organic nitrogen cycling in oceans. The nitrogen storage strategies of dinoflagellates are also vital to their symbiosis with corals, where organic nitrogen translocated from dinoflagellates enables coral reefs to thrive in nutrient-deficient waters.

The ability of dinoflagellates to crystallize nitrogen heterocycles rapidly from aqueous solutions is striking given that these sparingly soluble molecules require extreme pH values or organic solvents for recrystallization in vitro. The results show how microalgae may be exploited as cellular factories for producing molecular crystals from aqueous solutions, with possible further applications in the crystallization of pharmaceuticals and bioremediation of toxicants.