Exploring Microalgae as Cellular Factories for Molecular Crystals

Objective

Until now, the field of organic biomineralization has focused on the optical functions of organic crystals in animals. However, the recent discovery that purine crystals are widespread in unicellular microalgae is a paradigm shift in this field. In contrast to animals, microalgae use the nitrogen-rich crystals as dense, metabolically inert nitrogen reserves, to overcome deficiencies in environmental nitrogen. Almost nothing is known about the chemistry of these crystals, their formation, or the wider implications of their nitrogen storage functions on microalgae behavior. Our overarching goal is to understand microscale molecular crystallization in microalgae and its impact on macroscale ecological phenomena and the biotechnological production of optically functional crystals. We first elucidate the structures and functions of uncharacterized purine crystals which are abundant in microalgae. By controlling the nitrogen content of cultures, we exploit the ability to induce crystallization in microalgae using live cell, and correlative light-electron imaging to couple chemical and morphological properties of crystal formation. Combined with cryo-electron microscopy and chemical analyses, we determine the locations and functions of crystal-regulating biomolecules and elucidate how insoluble guanine molecules are rapidly crystallized and dissolved in the cell. Knowledge of crystallization is then harnessed to manipulate microalgal cells as crystal-forming factories to biosynthesize optically functional crystals using bioreactor cultures. Finally, we test the hypothesis that the nitrogen-storage function of crystals in dinoflagellates may serve to prolong their growth in seasonal and harmful algal blooms. Our exploration of crystallization in microalgae will transform our knowledge of microscale organic biomineralization and will contribute to understanding the macroscale impact of molecular crystals on ocean ecosystems and biotechnology – a new frontier in the field.