Using X-ray free-electron lasers for spectroscopy of molecular catalysts and metalloenzymes

Bergmann, Uwe; Kern, Jan; Schoenlein, R. W.; Wernet, Philippe; Yachandra, Vittal K.; Yano, Junko

doi:10.1038/s42254-021-00289-3

Cited by 82 publications

(79 citation statements)

References 184 publications

(236 reference statements)

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“…Exciting developments in time-resolved structural techniques have also been reported, particularly on light-triggered systems such as Photosystem II (PSII). 7 Despite these impressive experimental developments, it still remains highly challenging to probe how and why a certain reaction intermediate results in given chemical or structural changes. To this end, multiscale simulations provide a powerful approach to computationally resolve the functional dynamics, energetics, and structural changes at a single molecule level and thus to probe molecular mechanisms in biological energy conversion.…”

Section: Introductionmentioning

confidence: 99%

“…While methods of structural biology, in particular, X-ray crystallography and cryo-electron microscopy (cryoEM), can resolve static structures of the protein complexes at an atomistic resolution, different spectroscopic techniques are often required to experimentally determine the dynamics along the biochemical reaction cycle. Exciting developments in time-resolved structural techniques have also been reported, particularly on light-triggered systems such as Photosystem II (PSII) . Despite these impressive experimental developments, it still remains highly challenging to probe how and why a certain reaction intermediate results in given chemical or structural changes.…”

Section: Introductionmentioning

confidence: 99%

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Resolving Chemical Dynamics in Biological Energy Conversion: Long-Range Proton-Coupled Electron Transfer in Respiratory Complex I

Kaila

2021

Acc. Chem. Res.

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Conspectus Biological energy conversion is catalyzed by membrane-bound proteins that transduce chemical or light energy into energy forms that power endergonic processes in the cell. At a molecular level, these catalytic processes involve elementary electron-, proton-, charge-, and energy-transfer reactions that take place in the intricate molecular machineries of cell respiration and photosynthesis. Recent developments in structural biology, particularly cryo-electron microscopy (cryoEM), have resolved the molecular architecture of several energy transducing proteins, but detailed mechanistic principles of their charge transfer reactions still remain poorly understood and a major challenge for modern biochemical research. To this end, multiscale molecular simulations provide a powerful approach to probe mechanistic principles on a broad range of time scales (femtoseconds to milliseconds) and spatial resolutions (10 1 –10 6 atoms), although technical challenges also require balancing between the computational accuracy, cost, and approximations introduced within the model. Here we discuss how the combination of atomistic (aMD) and hybrid quantum/classical molecular dynamics (QM/MM MD) simulations with free energy (FE) sampling methods can be used to probe mechanistic principles of enzymes responsible for biological energy conversion. We present mechanistic explorations of long-range proton-coupled electron transfer (PCET) dynamics in the highly intricate respiratory chain enzyme Complex I, which functions as a redox-driven proton pump in bacterial and mitochondrial respiratory chains by catalyzing a 300 Å fully reversible PCET process. This process is initiated by a hydride (H – ) transfer between NADH and FMN, followed by long-range (>100 Å) electron transfer along a wire of 8 FeS centers leading to a quinone biding site. The reduction of the quinone to quinol initiates dissociation of the latter to a second membrane-bound binding site, and triggers proton pumping across the membrane domain of complex I, in subunits up to 200 Å away from the active site. Our simulations across different size and time scales suggest that transient charge transfer reactions lead to changes in the internal hydration state of key regions, local electric fields, and the conformation of conserved ion pairs, which in turn modulate the dynamics of functional steps along the reaction cycle. Similar functional principles, which operate on much shorter length scales, are also found in some unrelated proteins, suggesting that enzymes may employ conserved principles in the catalysis of biological energy transduction processes.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Resolving Chemical Dynamics in Biological Energy Conversion: Long-Range Proton-Coupled Electron Transfer in Respiratory Complex I

Kaila

2021

Acc. Chem. Res.

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“…[76] XAS is also sensitive to some details of the electronic structure, in particular, the oxidation state of metals can be determined, [77,78] which can be complemented by X-ray emission experiments that are sensitive to both spin and oxidation states. [76,[79][80][81] Depending on the required time resolution, pump-probe XAS data acquisition can be performed at synchrotron sources by gating the detector to one X-ray pulse (which allows getting ~100 ps resolution) [82,83] or by measuring the arrival time of many X-ray pulses (pumpsequential-probes method with ~20 ns resolution). [84] At X-ray free electron lasers experiments can be performed in the time range which starts from tens of femtoseconds, which is possible due to shorter X-ray pulses.…”

Section: Pump-probe Xas Study Of Mononuclear Cu Complexesmentioning

confidence: 99%

“…Depending on the required time resolution, pump‐probe XAS data acquisition can be performed at synchrotron sources by gating the detector to one X‐ray pulse (which allows getting ∼100 ps resolution) [82,83] or by measuring the arrival time of many X‐ray pulses (pump‐sequential‐probes method with ∼20 ns resolution) [84] . At X‐ray free electron lasers experiments can be performed in the time range which starts from tens of femtoseconds, which is possible due to shorter X‐ray pulses [80] . There are also other techniques to produce such ultrafast X‐ray pulses, including slicing [85] low‐α and coherent harmonic generation at synchrotrons, [86] high harmonic generation, [87] plasma sources [88] and betatron sources [89] at lasers.…”

Section: Pump‐probe Xas Study Of Mononuclear Cu Complexesmentioning

confidence: 99%

Time‐Resolved X‐Ray Spectroscopy to Study Luminophores with Relevance for OLEDs

Vogt

Smolentsev

2022

ChemPhotoChem

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Organic light-emitting diodes (OLEDs) are employed in innovative display technologies and have the potential to be used widely in large area lighting. Luminophores containing 4d or 5d metals are efficient in electro-luminescent devices due to their phosphorescent properties but are scarce and expensive. Alternatives take advantage of temperature-activated delayed fluorescence (TADF), e. g. in Cu(I) complexes. We show modern X-ray spectroscopy methods exemplified on Ru, Ir and Cu-based luminophores offering insight into the capabilities of such techniques to researchers from various fields. Knowledge of structural rearrangements in the excited state is crucial to understand non-radiative energy losses and to develop efficient luminophores. Pump-probe X-ray absorption spectroscopy (XAS) gives information about the molecular structure in the excited state and the electronic structure. We show how this information can be complemented with X-ray emission spectroscopy at X-ray free-electron lasers (XFEL) and discuss the potential of time-resolved X-ray excited optical luminescence (TR-XEOL) to provide additional selectivity of XAS to luminescent sites.

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“…Revealing the catalytic molecular mechanism and their corresponding statistical thermodynamic information is not only a central issue in catalytic science, but also provide a useful guide for the further rational design of the efficient catalytic processes. [1][2][3][4] Although an enormous amount of experimental effort has been conducted for molecular mechanism in heterogeneous catalysis, [5][6][7][8] there is still experimental technical difficulties of obtaining molecular information directly. Theoretical and computational tools thus have become an indispensable approach for revealing the molecular details as well as the thermodynamics in catalysis.…”

Section: Introductionmentioning

confidence: 99%

Efficient Dynamic Computational Strategy for Heterogeneous Catalysis Based on Neural Network Potential Energy Surface: A Case Study of Temperature-Dependent Thermodynamics and Kinetics for the Chemisorbed on-surface CO

Chen

Tan

Shen

et al. 2021

Preprint

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As a favorable alternative and complement of experimental techniques, computational tools on top of ab initio calculations have played an indispensable role in revealing the molecular details, thermodynamics and kinetics in catalytic reactions. The static computational strategy, which recovers the reaction thermodynamics and kinetics based on the calculations of a few stationary geometries at zero temperature and some ideal statistic mechanics models, is the most popular approach in theoretical catalysis due to its simplicity. In comparison, the ab initio molecular dynamics (AIMD) is a well-tested approach to provide more precise descriptions of catalytic processes, however, experiencing a significantly expensive computational cost in the direct ab initio calculation of potential energy and gradients. Here we proposed a highly efficient dynamic computational strategy for the calculation of thermodynamic and kinetic properties in heterogeneous catalysis on the basis of neural network potential energy surface (NN PES) and MD simulations. Taking CO adsorbate on Ru(0001) surface as the illustrative model catalytic system, we demonstrated that our NN-PES-based MD simulations can efficiently generate the reliable smooth two-dimensional potential-of-mean-force (2-D PMF) surfaces in a wide range of temperatures (from 300 to 900 K), and thus temperature-dependent thermodynamic properties can be obtained in a comprehensive investigation on the whole PMF surface rather than a rough estimation using ideal models based on a few optimized geometries. Moreover, MD simulations offer an effective way to describe the surface kinetics such as the CO adsorbate on-surface movement, which goes beyond the most popular static estimation based on calculated free energy barrier and transition state theory (TST). By comparing the results obtained in the dynamic and static approaches, we further revealed that the dynamic strategy significantly improves the predictions of both thermodynamic and kinetic properties as compared to the popular ideal statistic mechanics approaches such as harmonic analysis and TST. It is expected that this accurate yet efficient dynamic strategy can be a powerful tool in understanding reaction mechanisms and reactivity of a catalytic surface system, and further guides the rational design of heterogeneous catalysts.

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Using X-ray free-electron lasers for spectroscopy of molecular catalysts and metalloenzymes

Cited by 82 publications

References 184 publications

Resolving Chemical Dynamics in Biological Energy Conversion: Long-Range Proton-Coupled Electron Transfer in Respiratory Complex I

Resolving Chemical Dynamics in Biological Energy Conversion: Long-Range Proton-Coupled Electron Transfer in Respiratory Complex I

Time‐Resolved X‐Ray Spectroscopy to Study Luminophores with Relevance for OLEDs

Efficient Dynamic Computational Strategy for Heterogeneous Catalysis Based on Neural Network Potential Energy Surface: A Case Study of Temperature-Dependent Thermodynamics and Kinetics for the Chemisorbed on-surface CO

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