Crystalline materials built from small-molecule building blocks are promising for diverse applications, but characterizing their dynamic structural responses to stimuli remains a challenge. While techniques like low-temperature photocrystallography exist, they lack the temporal resolution to capture ultrafast processes. Femtosecond X-ray and electron diffraction can provide some information, but full three-dimensional electron density (ED) maps visualizing atomic positions require the collection of nearly all Bragg spots, a feat not always achievable with these methods. Time-resolved crystallography at synchrotron sources offers ~100 ps resolution but struggles with irreversible or slow reactions and those faster than 100 ps. Time-resolved serial femtosecond crystallography (TR-SFX), successful in visualizing protein dynamics, offers the high temporal and spatial resolution needed to address these limitations. However, TR-SFX has not been applied to non-biological crystalline small molecules due to challenges such as smaller lattice constants, leading to sparser Bragg peaks, and higher absorption cross-sections, resulting in weaker photoinduced signals. This study aimed to overcome these challenges and apply TR-SFX to a metal-organic framework (MOF) to elucidate its structural dynamics.

The literature extensively explores the structures and properties of novel crystalline materials composed of organic, inorganic, or organometallic building blocks, highlighting their applications in gas capture and separation. Past structural characterization relied on comparing static structures before and after stimulus application. Photocrystallography at low temperatures has been used to capture reaction intermediates in organic and inorganic reactions. However, the need for a high-temporal resolution structural probe for studying the ultrafast structural dynamics of crystalline small-molecule materials remains. While femtosecond X-ray and electron diffraction techniques have been used, they offer limited information, lacking the capability to construct full 3D ED maps. Time-resolved crystallography at synchrotron sources, although capable of probing chemical systems, is limited when dealing with fast, irreversible, or slow-recovery reactions. TR-SFX, employed successfully for protein studies, holds promise for overcoming these limitations, yet its application to small molecule crystals remained largely unexplored before this study, despite a recent report on static SFX.

This research employed TR-SFX to study PCN-224(Fe)-CO, an iron-porphyrinic zirconium MOF optimized for TR-SFX analysis. A fixed-target sample holder, offering advantages in sample consumption and chemical compatibility, was used instead of the typical injector system. Micro-sized PCN-224(Fe)-CO crystals (10–20 µm) were placed on the holder, and a 400 nm femtosecond laser pulse triggered photoinduced CO dissociation. A femtosecond X-ray pulse from an XFEL then captured the diffraction pattern at various time delays (33 delays, significantly more than previous TR-SFX studies). High X-ray energy (14.5 keV) was used to increase the number of detectable Bragg peaks, compensating for the sparser peaks characteristic of small-molecule crystals. Data processing involved using Cheetah for image selection and CrystFEL for indexing, integration, and merging. Structure refinement employed SHELXT and SHELXL, addressing crystallographic disorder using restraints. The SQUEEZE option in PLATON handled the residual electron density from disordered solvents or gas. Difference electron density (DED) maps were generated to visualize structural changes at each time delay. Singular value decomposition (SVD) was applied to quantitatively analyze DED maps, extracting time-invariant features and time profiles. Kinetic modeling, using a three-species model (oscillatory, transient, and vibrationally hot structures), allowed the extraction of species-associated DED (SADED) maps. Extrapolated maps were generated from SADED maps and the ground-state structure to obtain the refined structures of the three structural species. The photoconversion yields were extrapolated to 100% to obtain the structures of pure forms of the three species.

The TR-SFX data revealed a trifurcating structural pathway following photoexcitation. First, within the instrument response function (<200 fs), coherent oscillations of both Zr and Fe atoms occurred. This oscillatory structure (Iosc) featured enhanced doming of the Fe porphyrin and disordering of the Zr atoms along the d-axis, with a period of 5.55 ps. Second, a transient structure (It) formed instantaneously and decayed with a time constant of 47.1 ps. It showed amplified doming and disordering compared to the ground state, suggesting a strong coupling between the porphyrin and the Zr node. Finally, a vibrationally hot structure (Ihot) emerged, characterized by isotropic structural disorder and persisting to 3 ns. This structure showed that the original metal positions had strong negative densities surrounded by strong positive densities. The thermal contribution to this structure rose with two time constants of 1.143 and 11.32 ps. The analysis also revealed a strong correlation between Zr-Zr distance and the degree of Fe doming, indicating a close coupling between the movements of these two components. The oscillatory motion of 0.18 THz is considerably slow for small molecules, and was assigned to a phonon mode in the solid sample. The study observed a large number of vibrationally hot structures which is rarely seen in protein crystals due to the efficient heat absorption from water and buffer molecules in protein crystals.

The findings demonstrate that the initial photoinduced CO dissociation from the Fe porphyrin triggers organized anisotropic movements in both the Fe porphyrin and the distant Zr node. These movements exhibit coherent oscillations, a rarely observed phenomenon directly visualized in a DED map in time-resolved crystallography. The slow oscillatory motion of 5.55 ps is attributed to a phonon mode within the MOF structure. The subsequent transition to a vibrationally hot structure underscores the efficient energy transfer within the MOF and the absence of efficient heat dissipation mechanisms compared to protein crystals. The three distinct pathways, oscillatory, transient, and vibrationally hot, provide a comprehensive picture of the ultrafast structural dynamics within this MOF system, highlighting the interplay between local photoexcitation and global structural responses.

This study successfully applied TR-SFX to a non-protein chemical system, a metal-organic framework, revealing intricate ultrafast structural dynamics. The observation of coherent oscillations and a vibrationally hot state significantly extends the applications of TR-SFX beyond protein studies. Future research could explore the applicability of TR-SFX to other MOFs and porous materials, examining the influence of different stimuli and framework architectures on dynamic behavior.

The study focused on a specific MOF system and specific excitation conditions (400 nm light). The generalizability of these findings to other MOFs or different excitation wavelengths needs further investigation. The modeling of the vibrationally hot structure relied on simulations, and experimental validation might strengthen the conclusions.