The mechanism driving a solid-solid phase transition in a biomacromolecular crystal.

Saminathan Ramakrishnan,William F. Heinz,Xiaobing Zuo,Yun-Xing Wang,Jason R. Stagno,Ping Yu

doi:10.1107/s2052252521004826

Abstract

Solid-solid phase transitions (SSPTs) occur between distinguishable crystalline forms. Because of their importance in application and theory in materials science and condensed-matter physics, SSPTs have been studied most extensively in metallic alloys, inorganic salts and small organic molecular crystals, but much less so in biomacromolecular crystals. In general, the mechanisms of SSPTs at the atomic and molecular levels are not well understood. Here, the ordered molecular rearrangements in biomacromolecular crystals of the adenine riboswitch aptamer are described using real-time serial crystallography and solution atomic force microscopy. Large, ligand-induced conformational changes drive the initial phase transition from the apo unit cell (AUC) to the trans unit cell 1 (TUC1). During this transition, coaxial stacking of P1 duplexes becomes the dominant packing interface, whereas P2-P2 interactions are almost completely disrupted, resulting in 'floating' layers of molecules. The coupling points in TUC1 and their local conformational flexibility allow the molecules to reorganize to achieve the more densely packed and energetically favorable bound unit cell (BUC). This study thus reveals the interplay between the conformational changes and the crystal phases - the underlying mechanism that drives the phase transition. Using polarized video microscopy to monitor SSPTs in small crystals at high ligand concentration, the time window during which the major conformational changes take place was identified, and the in crystallo kinetics have been simulated. Together, these results provide the spatiotemporal information necessary for informing time-resolved crystallography experiments. Moreover, this study illustrates a practical approach to characterization of SSPTs in transparent crystals.

Highlights

In both organic and inorganic crystals, rearrangements of atoms or small molecules occur in diffusionless solid–solid phase transitions (SSPTs), which are generally triggered by temperature, humidity, pressure or mechanical stress (Commins et al, 2016; Anwar & Zahn, 2017)
atomic force microscopy (AFM) is consistent with the crystal structure [Fig. 1(a)] which, when superimposed onto the apo unit cell (AUC) AFM topography [Fig. S3(a)], highlights the distinct crystal packing interfaces
The molecules in the ac plane of AUC are coupled predominantly through a symmetrical network of hydrogen bonds and van der Waals (VDW) contacts involving residues 29 and 42–45, located in the P2 stems of adjacent molecules [Fig. 1(a), bottom]

Summary

Introduction

In both organic and inorganic crystals, rearrangements of atoms or small molecules occur in diffusionless solid–solid phase transitions (SSPTs), which are generally triggered by temperature, humidity, pressure or mechanical stress (Commins et al, 2016; Anwar & Zahn, 2017). Well known examples are phase changes in shape memory alloys caused by temperature variation (Otsuka & Wayman, 1998), or in small organic molecular crystals by heat or light exposure (Etter & Siedle, 1983; Skoko et al, 2010; Smets et al, 2020). Mechanisms of SSPTs in organic and inorganic crystals at the molecular and atomic levels are relatively poorly understood due to technical challenges, but frequently involve dislocation generation and motion. A very recent study of organic molecular crystals illustrates the cooperative motion in phase transitions (Smets et al, 2020)

Methods

Results

Conclusion