The variability in the structural and functional properties of coccolith base plates

Abstract

Biomineralization processes exert varying levels of control over crystallization, ranging from poorly ordered polycrystalline arrays to intricately shaped single crystals. Coccoliths, calcified scales formed by unicellular algae, are a model for a highly controlled crystallization process. The coccolith crystals nucleate next to an organic oval structure that was termed the base plate, leading to the assumption that it is responsible for the oriented nucleation of the crystals via stereochemical interactions. In recent years, several works focusing on a well-characterized model species demonstrated a fundamental role for indirect interactions that facilitate coccolith crystallization. Here, we developed the tools to extract the base plates from five different species, giving the opportunity to systematically explore the relations between base plate and coccolith properties. We used multiple imaging techniques to evaluate the structural and chemical features of the base plates under native hydrated conditions. The results show a wide range of properties, overlaid on a common rudimentary scaffold that lacks any detectable structural or chemical motifs that can explain direct nucleation control. This work emphasizes that it is the combination between the base plate and the chemical environment inside the cell that cooperatively facilitate the exquisite control over the crystallization process. STATEMENT OF SIGNIFICANCE: Biological organic scaffolds can serve as functional surfaces that guide the formation of inorganic materials. However, in many cases the specific interactions that facilitate such tight regulation are complex and not fully understood. In this work, we elucidate the architecture of such amodel biological template, an organic scale that directs the assembly of exquisite crystalline arrays of marine microalgae. By using cryo electron microscopy, we reveal the native state organization of these scales from several species. The observed similarities and differences allow us to propose that the chemical microenvironment, rather than stereochemical matching, is the pivotal regulator of the process.

Keywords: Biomineralization; Calcite; Coccoliths; Cryo electron tomography; Crystallization.