Periodic Reporting for period 5 - NONABVD (Nonadiabaticity in Biomolecular Vibrational Dynamics)
Reporting period: 2023-12-01 to 2024-12-31
The ERC Starting Grant project NONABVD aims at the fundamental understanding of ultrafast biomolecular vibrational dynamics in the mid-IR/THz region. We investigate the impact of nonadiabatic effects in dipolar liquids, within the confinement of protein environments and at biological interfaces. In such scenarios, the coupling to the aqueous environment occurs through a variety of noncovalent interactions that determine the properties of elementary charge carriers (like excess protons and hydrated electrons), or of the polyanionic biomolecules (like DNA or RNA). Local structures are determined by hydrogen bonds with water molecules and complemented by non-specific electrostatic and many-body interactions. The structural fluctuations of the water shell result in fluctuating Coulomb forces and in a breaking and reformation of hydrogen bonds. The understanding of these processes via underlying interactions is of fundamental importance with applications covering microscopic descriptions of elementary proton transfer reactions, mechanisms of energy dissipation upon vibrational excitation and solvation dynamics in biomolecules.
The NONABVD project transfers paradigms of nonadiabatic electronic relaxation to the low energy mid-IR/THz domain of biomolecular vibrational dynamics. The approach provides a description of microscopic phenomena like structural fluctuations, vibrational lifetimes and dissipation of excess energy and fully accounts for the strong impact of the fluctuating environment on biomolecular structure and dynamics. The concise theoretical description of proton or electron solvation and transfer processes in the vicinity of biological interfaces is highly relevant as microscopic foundation of cell respiration and technological applications, like fuel cells. Our findings demonstrated for a broad range of scenarios the occurrence of non-adiabaticity as general physical phenomena in the non-equilibrium relaxation dynamics subject to environment fluctuations.
The NONABVD project transfers paradigms of nonadiabatic electronic relaxation to the low energy mid-IR/THz domain of biomolecular vibrational dynamics. The approach provides a description of microscopic phenomena like structural fluctuations, vibrational lifetimes and dissipation of excess energy and fully accounts for the strong impact of the fluctuating environment on biomolecular structure and dynamics. The concise theoretical description of proton or electron solvation and transfer processes in the vicinity of biological interfaces is highly relevant as microscopic foundation of cell respiration and technological applications, like fuel cells. Our findings demonstrated for a broad range of scenarios the occurrence of non-adiabaticity as general physical phenomena in the non-equilibrium relaxation dynamics subject to environment fluctuations.
The project NONABVD addressed manifestations of vibrational nonadiabaticity relevant for liquid phase environments and biomolecules. In this context, the quantification of solvation structures and dynamics of elementary charge carriers, as well as a characterization of electric large amplitude field fluctuations is of outstanding relevance for defining the dynamical properties. Within the project we could obtain novel, unprecedented insight into (i) biomolecular electrostatics, (ii) proton and ion solvation structures as well as their interactions with the fluctuating environment, (iii) coherence effects in the solvation dynamics of hydrated electrons, and (iv) the importance of non-Markovianity in energy relaxation subject to complex environments.
The characterization of the phosphate-water interface established a novel detection scheme of phosphate counter-ion interactions that allows the quantification of electrostatics at biomolecular interfaces. The theoretically predicted infrared detection scheme of phosphate-contact ion interactions relies on the particular sensitivity to microscopic differences in hydration structure and establishes new experimental data of contact ion pair formation. The results underline the potential of nonlinear 2D-IR spectroscopy as an analytical probe of phosphate-ion interactions in complex biomolecular systems. The results are of large interdisciplinary importance for ongoing collaborative research, like the DFG centre SFB1309 – Chemical Biology of Epigenetic Modification and the DFG cluster of excellence e-Conversion.
The accurate simulation of dissipative quantum dynamics subject to a non-Markovian environment poses persistent numerical challenges. We have developed a scalable distributed memory implementation of the Mask Assisted Coarse Graining of Influence Coefficients (MACGIC) - Quasi-Adiabatic Propagator Path Integral (-QUAPI) simulation method that allows to exploit the memory resources of multiple compute nodes. The novel algorithm mitigates the memory bottleneck of the method and numerical efficiency arises from a hash-based bookkeeping of interfering quantum pathways (hMACGIC-QUAPI), yielding a general purpose simulation program for quantum dynamics subject to non-Markovian environments.
Within the project a new general purpose software for dissipative quantum dynamics was developed. Dissemination of the results lead to 23 publications, presentations at international conferences and the Coblentz Award.
The characterization of the phosphate-water interface established a novel detection scheme of phosphate counter-ion interactions that allows the quantification of electrostatics at biomolecular interfaces. The theoretically predicted infrared detection scheme of phosphate-contact ion interactions relies on the particular sensitivity to microscopic differences in hydration structure and establishes new experimental data of contact ion pair formation. The results underline the potential of nonlinear 2D-IR spectroscopy as an analytical probe of phosphate-ion interactions in complex biomolecular systems. The results are of large interdisciplinary importance for ongoing collaborative research, like the DFG centre SFB1309 – Chemical Biology of Epigenetic Modification and the DFG cluster of excellence e-Conversion.
The accurate simulation of dissipative quantum dynamics subject to a non-Markovian environment poses persistent numerical challenges. We have developed a scalable distributed memory implementation of the Mask Assisted Coarse Graining of Influence Coefficients (MACGIC) - Quasi-Adiabatic Propagator Path Integral (-QUAPI) simulation method that allows to exploit the memory resources of multiple compute nodes. The novel algorithm mitigates the memory bottleneck of the method and numerical efficiency arises from a hash-based bookkeeping of interfering quantum pathways (hMACGIC-QUAPI), yielding a general purpose simulation program for quantum dynamics subject to non-Markovian environments.
Within the project a new general purpose software for dissipative quantum dynamics was developed. Dissemination of the results lead to 23 publications, presentations at international conferences and the Coblentz Award.
Magnesium contact ions stabilize the macromolecular structure of transfer RNA [DOI: 10.1021/acs.jpcb.0c08966]: We have identified contact pairs of positively charged magnesium ions and negatively charged phosphate groups as a decisive structural element for minimizing the electrostatic energy of tRNA and, thus, stabilizing its tertiary structure. The results give detailed insight in the electric properties of a key biomolecule and underscore the relevance of molecular probes for elucidating the relevant molecular interactions.
Quantum state mixing in photobiology [DOI: 10.1073/pnas.2319676121]: The excited state character governing the reaction dynamics of the protonated Schiff base in bacteriorhodopsin, a light induced proton pump, has remained controversial. We could show that nonadiabatic mixing of S1 and S2 excited states and temporal averaging over the first 120 fs of the ultrafast excited state dynamics account for the measured dipole changes in THz Stark spectroscopy. On the timescale of the experiment, the protein environment of the chromophore is practically frozen, providing a clear view on its electronic properties and revealing a quantum mixing of states as a key mechanism in molecular systems relevant for chemistry and biology.
Magnesium ions slow down water dynamics on short length scales [DOI: 10.1021/acsphyschemau.2c00034]: Liquid water, the native medium for biochemical processes, responds to the presence of charged ions by changing its local structure. The influence of ions on water is usually classified via the Hofmeister series which ranks ions based on their ability to structure the water around them. We could demonstrate a significantly more complex influence of ions on the dynamics of surrounding water molecules. The presence of Mg2+ ions reduces the ultrafast fluctuations of the water shell around a sulfate ion, leading to a specific slowdown in the solvation dynamics of hydrated MgSO4. Contrary to the widespread account in the literature, the described effects are of short range and limited to the first 1-2 water layers around the sulfate ion.
Terahertz waves from electrons oscillating in liquid water [DOI: 10.1103/physrevlett.126.097401]: Electrons in water are a prototypical quantum system in interaction with a fluctuating environment. Their non-equilibrium generation leads to long-lived oscillatory dynamics in the terahertz range with a oscillation frequency determined by the local electric field the liquid environment. Surprising is the comparably weak damping of the oscillations which points to a weak interaction with the fluctuating environment. The results suggest a polaron picture of solvated electrons, i.e. a quasi-particle of coupled motions of the electron and the surrounding water shell.
Quantum state mixing in photobiology [DOI: 10.1073/pnas.2319676121]: The excited state character governing the reaction dynamics of the protonated Schiff base in bacteriorhodopsin, a light induced proton pump, has remained controversial. We could show that nonadiabatic mixing of S1 and S2 excited states and temporal averaging over the first 120 fs of the ultrafast excited state dynamics account for the measured dipole changes in THz Stark spectroscopy. On the timescale of the experiment, the protein environment of the chromophore is practically frozen, providing a clear view on its electronic properties and revealing a quantum mixing of states as a key mechanism in molecular systems relevant for chemistry and biology.
Magnesium ions slow down water dynamics on short length scales [DOI: 10.1021/acsphyschemau.2c00034]: Liquid water, the native medium for biochemical processes, responds to the presence of charged ions by changing its local structure. The influence of ions on water is usually classified via the Hofmeister series which ranks ions based on their ability to structure the water around them. We could demonstrate a significantly more complex influence of ions on the dynamics of surrounding water molecules. The presence of Mg2+ ions reduces the ultrafast fluctuations of the water shell around a sulfate ion, leading to a specific slowdown in the solvation dynamics of hydrated MgSO4. Contrary to the widespread account in the literature, the described effects are of short range and limited to the first 1-2 water layers around the sulfate ion.
Terahertz waves from electrons oscillating in liquid water [DOI: 10.1103/physrevlett.126.097401]: Electrons in water are a prototypical quantum system in interaction with a fluctuating environment. Their non-equilibrium generation leads to long-lived oscillatory dynamics in the terahertz range with a oscillation frequency determined by the local electric field the liquid environment. Surprising is the comparably weak damping of the oscillations which points to a weak interaction with the fluctuating environment. The results suggest a polaron picture of solvated electrons, i.e. a quasi-particle of coupled motions of the electron and the surrounding water shell.