Good vibrations in enzyme-catalysed reactions

Hay, Sam; Scrutton, Nigel S.

doi:10.1038/nchem.1223

Cited by 274 publications

(336 citation statements)

References 69 publications

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“…Besides its implications on PT on aqueous systems, the phenomena we observe bear similar features to important biological systems. In particular, collective vibrations have recently been recognized as playing a possible role in promoting hydrogen transfer in enzymes (37), which is crucial for catalysis. In addition, the fundamental aspects raised in this report are likely to open up new directions in the role of the water network in phenomena associated with the hydration of ions (38) and macromolecules such as proteins and DNA.…”

Section: Resultsmentioning

confidence: 99%

Proton transfer through the water gossamer

Hassanali

Giberti

Cuny

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

348

421

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The diffusion of protons through water is understood within the framework of the Grotthuss mechanism, which requires that they undergo structural diffusion in a stepwise manner throughout the water network. Despite long study, this picture oversimplifies and neglects the complexity of the supramolecular structure of water. We use first-principles simulations and demonstrate that the currently accepted picture of proton diffusion is in need of revision. We show that proton and hydroxide diffusion occurs through periods of intense activity involving concerted proton hopping followed by periods of rest. The picture that emerges is that proton transfer is a multiscale and multidynamical process involving a broader distribution of pathways and timescales than currently assumed. To rationalize these phenomena, we look at the 3D water network as a distribution of closed directed rings, which reveals the presence of medium-range directional correlations in the liquid. One of the natural consequences of this feature is that both the hydronium and hydroxide ion are decorated with proton wires. These wires serve as conduits for long proton jumps over several hydrogen bonds.T he mechanism by which protons move through water is at the heart of acid-base chemistry reactions. Understanding the reaction coordinates of this process has been one of the most challenging problems in physical chemistry due to the sheer complexity of water's hydrogen bond network (1-4). Developing a molecular basis for these phenomena is of great relevance in energy conversion applications such as in the design of efficient fuel cells (5). Over 200 y ago, von Grotthuss proposed a mechanism by which water would undergo electrolytic decomposition (6). He imagined that proton conduction involved the collective shuttling of hydrogen atoms along water wires. The early 20th century found many of the great scientists of the time developing conceptual models to understand the properties of water and its constituent ions (7,8). Detailed insights into the mechanisms of proton transfer (PT) came much later from a combination of both ab initio molecular dynamics (AIMD) simulations (3, 9-13) and force-field approaches based on the empirical valence bond formalism (14-16). The current textbook picture of the Grotthuss mechanism that has resulted from these studies involves a stepwise hopping of the proton from one water molecule to the next (1,17,18). This process occurs on a timescale of 1-2 ps. For a successful transfer, the model requires solvent reorganization around the proton-receiving species to develop a coordination pattern like that of the species it will convert to, a process known as presolvation. In all of these characterizations of the Grotthuss mechanism, the role of the connectivity of the water network was not brought to the forefront (3, 19).Sometimes PT has also been thought to take on coherent character involving jumps of several protons simultaneously. In this spirit, Eigen (20) suggested that the proton could delocalize over extended hydrogen...

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Section: Resultsmentioning

confidence: 99%

Proton transfer through the water gossamer

Hassanali

Giberti

Cuny

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

348

421

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“…However, enzymes (12)(13)(14)(15)(16) are also very important catalytic systems, and recent studies have focused on how to synthesize pure enzymes as well as on how to look for similarities between enzymes and all three catalytic systems on the molecular scale. For example, it is known that, when enzymes are immobilized on a surface, they gain the reusability and ease of separation seen in heterogeneous catalysts, as well as in some cases becoming more stable to wider pH and temperature ranges (61)(62)(63).…”

Section: Hybrid Systems: Outlookmentioning

confidence: 99%

“…The first is in the development of nanomaterials science (1-4), which has made it possible to synthesize metallic (5-7), bimetallic, and core-shell nanoparticles (8,9), mesoporous metal oxides (10,11), and enzymes (12)(13)(14)(15)(16) in the nanocatalytic range between 0.8 and 10 nm. The second innovation is in the advancement of spectroscopy and microscopy instruments (17)(18)(19)(20)-including nonlinear laser optics (21), sum-frequency generation vibrational spectroscopy (22)(23)(24), and synchrotronbased instruments, such as ambient pressure X-ray photoelectron spectroscopy (8,(25)(26)(27), X-ray absorption near-edge structure, extended X-ray absorption fine structure (28)(29)(30), infrared (IR) and X-ray microspectroscopies (31), and high-pressure scanning tunneling microscopies (32,33)-that characterize catalysts at the atomic and molecular levels under reaction conditions (34).…”

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confidence: 99%

Molecular catalysis science: Perspective on unifying the fields of catalysis

Hurlburt

Sabyrov

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Colloidal chemistry is used to control the size, shape, morphology, and composition of metal nanoparticles. Model catalysts as such are applied to catalytic transformations in the three types of catalysts: heterogeneous, homogeneous, and enzymatic. Real-time dynamics of oxidation state, coordination, and bonding of nanoparticle catalysts are put under the microscope using surface techniques such as sumfrequency generation vibrational spectroscopy and ambient pressure X-ray photoelectron spectroscopy under catalytically relevant conditions. It was demonstrated that catalytic behavior and trends are strongly tied to oxidation state, the coordination number and crystallographic orientation of metal sites, and bonding and orientation of surface adsorbates. It was also found that catalytic performance can be tuned by carefully designing and fabricating catalysts from the bottom up. Homogeneous and heterogeneous catalysts, and likely enzymes, behave similarly at the molecular level. Unifying the fields of catalysis is the key to achieving the goal of 100% selectivity in catalysis.Two major breakthroughs have revolutionized molecular catalysis science over the last 20 y. The first is in the development of nanomaterials science (1-4), which has made it possible to synthesize metallic (5-7), bimetallic, and core-shell nanoparticles (8, 9), mesoporous metal oxides (10, 11), and enzymes (12-16) in the nanocatalytic range between 0.8 and 10 nm. The second innovation is in the advancement of spectroscopy and microscopy instruments (17-20)-including nonlinear laser optics (21), sum-frequency generation vibrational spectroscopy (22-24), and synchrotronbased instruments, such as ambient pressure X-ray photoelectron spectroscopy (8,(25)(26)(27), X-ray absorption near-edge structure, extended X-ray absorption fine structure (28-30), infrared (IR) and X-ray microspectroscopies (31), and high-pressure scanning tunneling microscopies (32, 33)-that characterize catalysts at the atomic and molecular levels under reaction conditions (34). Most of the studies that use these techniques focus on nanoscale technologies, such as catalytic energy conversion and information storage, which have reduced the size of transistors to below 25 nm (35).Catalysts are classified into three types-heterogeneous, homogeneous, and enzymatic-and, in most cases, range in size from 1 to 10 nm, which is even smaller than the transistors being developed by the latest size-fabrication technologies. Heterogeneous catalysts work in reaction systems with multiple phases (e.g., solid-gas or solid-liquid phase); homogeneous catalysts reside in the same phase as the reactants, almost always in the liquid phase; and enzymatic catalysts, which are most active in an aqueous solution, make use of active sites in proteins. The catalysis of chemical energy conversion provides ever-increasing selectivity in producing combustible hydrocarbons, gasoline, and diesel.The tenets that direct our catalysis research involve nanoparticle synthesis, characterization under reaction con...

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“…4) and slower time scales 5,31,32 and are often attributed to conformational (classical) distributions of the D-A distance 4,5,7,[33][34][35] . Other approaches 12,27,36 factor out and quantize the D-A vibration (~100 fs), as well as the much higher frequency (~10 fs) vibrational mode of the tunneling particle, which is a common feature in all analytical models (see Supplementary Discussion 4).…”

Section: Deep Tunneling Modelsmentioning

confidence: 99%

Wide-dynamic-range kinetic investigations of deep proton tunnelling in proteins

et al. 2016

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Abstract:Directional proton transport along "wires" that feed biochemical reactions in proteins is poorly understood. Amino acid residues with high pK a are seldom considered as active transport elements in such wires because of their large classical barrier for proton dissociation. Here we use the light-triggered proton wire of the green fluorescent protein (GFP) to study its ground electronic state proton transport kinetics, revealing a large temperature-dependent kinetic isotope effect. We show that "deep" proton tunneling between hydrogen-bonded oxygen atoms having a typical donor-acceptor distance of 2.7-2.8 Ǻ fully accounts for the rates at all temperatures, including the unexpectedly large value (2.5 10 9 s -1 ) found at room temperature. The rate limiting step in GFP is assigned to tunneling of the ionization-resistant serine hydroxyl proton. This suggests how high pK a residues within a proton wire can act as a "tunnel-diode" to kinetically trap protons and control the direction of proton flow.

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Good vibrations in enzyme-catalysed reactions

Cited by 274 publications

References 69 publications

Proton transfer through the water gossamer

Proton transfer through the water gossamer

Molecular catalysis science: Perspective on unifying the fields of catalysis

Wide-dynamic-range kinetic investigations of deep proton tunnelling in proteins

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