The mechanism driving a solid–solid phase transition in a biomacromolecular crystal
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 cry...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
International Union of Crystallography
2021-07-01
|
| Series: | IUCrJ |
| Subjects: | |
| Online Access: | http://scripts.iucr.org/cgi-bin/paper?S2052252521004826 |
| _version_ | 1828438087300022272 |
|---|---|
| author | Saminathan Ramakrishnan Jason R. Stagno William F. Heinz Xiaobing Zuo Ping Yu Yun-Xing Wang |
| author_facet | Saminathan Ramakrishnan Jason R. Stagno William F. Heinz Xiaobing Zuo Ping Yu Yun-Xing Wang |
| author_sort | Saminathan Ramakrishnan |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-10T19:57:44Z |
| format | Article |
| id | doaj.art-62ac725df50e4fca9bcbecbe66606c5d |
| institution | Directory Open Access Journal |
| issn | 2052-2525 |
| language | English |
| last_indexed | 2024-12-10T19:57:44Z |
| publishDate | 2021-07-01 |
| publisher | International Union of Crystallography |
| record_format | Article |
| series | IUCrJ |
| spelling | doaj.art-62ac725df50e4fca9bcbecbe66606c5d2022-12-22T01:35:36ZengInternational Union of CrystallographyIUCrJ2052-25252021-07-018465566410.1107/S2052252521004826lq5040The mechanism driving a solid–solid phase transition in a biomacromolecular crystalSaminathan Ramakrishnan0Jason R. Stagno1William F. Heinz2Xiaobing Zuo3Ping Yu4Yun-Xing Wang5Structural Biophysics Laboratory, Centre for Cancer Research, National Cancer Institute, Frederick, MD 21702, USAStructural Biophysics Laboratory, Centre for Cancer Research, National Cancer Institute, Frederick, MD 21702, USAOptical Microscopy and Analysis Laboratory, Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD 21702, USAX-ray Science Division, Argonne National Laboratory, Lemont, IL 60439, USAStructural Biophysics Laboratory, Centre for Cancer Research, National Cancer Institute, Frederick, MD 21702, USAStructural Biophysics Laboratory, Centre for Cancer Research, National Cancer Institute, Frederick, MD 21702, USASolid–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.http://scripts.iucr.org/cgi-bin/paper?S2052252521004826solid–solid phase transition mechanismstime-resolved crystallographyrna structural biologylarge conformational changes |
| spellingShingle | Saminathan Ramakrishnan Jason R. Stagno William F. Heinz Xiaobing Zuo Ping Yu Yun-Xing Wang The mechanism driving a solid–solid phase transition in a biomacromolecular crystal IUCrJ solid–solid phase transition mechanisms time-resolved crystallography rna structural biology large conformational changes |
| title | The mechanism driving a solid–solid phase transition in a biomacromolecular crystal |
| title_full | The mechanism driving a solid–solid phase transition in a biomacromolecular crystal |
| title_fullStr | The mechanism driving a solid–solid phase transition in a biomacromolecular crystal |
| title_full_unstemmed | The mechanism driving a solid–solid phase transition in a biomacromolecular crystal |
| title_short | The mechanism driving a solid–solid phase transition in a biomacromolecular crystal |
| title_sort | mechanism driving a solid solid phase transition in a biomacromolecular crystal |
| topic | solid–solid phase transition mechanisms time-resolved crystallography rna structural biology large conformational changes |
| url | http://scripts.iucr.org/cgi-bin/paper?S2052252521004826 |
| work_keys_str_mv | AT saminathanramakrishnan themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT jasonrstagno themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT williamfheinz themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT xiaobingzuo themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT pingyu themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT yunxingwang themechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT saminathanramakrishnan mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT jasonrstagno mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT williamfheinz mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT xiaobingzuo mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT pingyu mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal AT yunxingwang mechanismdrivingasolidsolidphasetransitioninabiomacromolecularcrystal |