Solvation Dynamics in the Molten Globule State of a Protein

Sen, Pratik; Mukherjee, Saptarshi; Dutta, Partha; Halder, Arnab; Mandal, Debabrata; Banerjee, Rajat; Roy, Siddhartha; Bhattacharyya, Kankan

doi:10.1021/jp036277d

Cited by 49 publications

(67 citation statements)

References 48 publications

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“…Indeed, using extrinsic probes with more longlived excited states, DSS decays of several nanoseconds have been reported. [38][39][40][41][42] According to our analysis, the decay time of the slow S W (t) component does not contain any information about protein hydration dynamics. It is therefore misleading to state that "we have determined the actual time scale of coupled water-protein fluctutations".…”

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confidence: 86%

Does the Dynamic Stokes Shift Report on Slow Protein Hydration Dynamics?

2009

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The time-dependent fluorescence frequency shift of protein-attached probes has a much slower decay than that for the free probe. The decay times, ranging from 10 ps to several nanoseconds, have been attributed to hydration water motions several orders of magnitude slower than those in the hydration shell of small solutes. This interpretation deviates strongly from the prevailing picture of protein hydration dynamics. We argue here that the slow decay in the fluorescence shift can be explained by a ubiquitous solvent polarization mechanism, with no need to invoke slow water motions or a dynamic coupling with protein motions. This mechanism can be qualitatively understood with the aid of a dielectric continuum model. We therefore conclude that the long decay times measured with time-dependent fluorescence spectroscopy contain no information about protein hydration dynamics.Many biological processes depend critically on the dynamical properties of the water-protein interface. During the past half century, a diverse array of techniques has therefore been recruited to the challenging task of quantitatively characterizing, under physiological solution conditions, the motions of water molecules in the protein hydration layer.1 The current picture, founded largely on 17 O NMR relaxation 2-5 and MD simulation [6][7][8][9][10][11] studies, reveals a dynamically heterogeneous hydration layer; a few water molecules spend long periods (up to ∼1 ns) trapped in surface pockets, while ∼90% of the interfacial water molecules, like those in the hydration shell of small organic solutes, suffer a mere two-fold average dynamical retardation as compared to bulk water. In recent years, this picture has been challenged by time-resolved fluorescence measurements, which seem to indicate that water motions in the hydration layer are slowed down by several orders of magnitude. [12][13][14][15][16][17][18][19][20][21][22] In this Letter, we argue that the long decay times seen by this technique reflect protein conformational fluctuations rather than hydration dynamics. There is thus no need to revise the prevailing picture of protein hydration dynamics.The fluorescence-detected dynamic Stokes shift (DSS) monitors the interaction energy of a fluorescent probe with its molecular environment. The charge distribution of the probe is altered by electronic excitation, and the ensuing readjustment of the environment is reflected in the time-dependent DSS. The DSS from a free probe in aqueous solution exhibits a sub-100 fs inertial decay of large amplitude, followed by a diffusive decay with a characteristic time of ∼1 ps. 23,24 In a dielectric model, the longer decay time corresponds to the dipolar longitudinal relaxation time of the solvent, which is 0.6 ps for bulk water at 298 K.When the probe is attached to a protein, the DSS exhibits one or more slowly decaying components in addition to the inertial decay (which is not always resolved) and a fast diffusive decay of a few picoseconds (corresponding to the ∼1 ps component of the free probe). Th...

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confidence: 86%

Does the Dynamic Stokes Shift Report on Slow Protein Hydration Dynamics?

2009

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“…LHI and LHII refer to light harvesting complexes I and II in photosynthetic purple bacteria. [33] (the "spin")which is coupled linearly to an infinite "bath" of harmonic oscillators. For biomolecular systems, the spin-boson model has previously been applied to electron transfer.…”

Section: Introductionmentioning

confidence: 99%

Quantum Dynamics of Electronic Excitations in Biomolecular Chromophores: Role of the Protein Environment and Solvent

2008

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We consider continuum dielectric models as minimal models to understand the effect of a surrounding globular protein and solvent on the quantum dynamics of electronic excitations in a biological chromophore. For these models we derive expressions for the frequency dependent spectral density which describes the coupling of the electronic levels in the chromophore to its environment. The magnitude and frequency dependence of the spectral density determines whether or not the quantum dynamics is coherent or incoherent, and thus whether on not one can observe quantum interference effects such as Rabi oscillations. We find the contributions to the spectral density from each component of the chromophore environment: the bulk solvent, protein, and water bound to the protein. The relative importance of each component to the quantum dynamics of the chromophore is determined by the time scale on which one is considering the dynamics. Our results provide a natural explanation and model for the different time scales observed in the spectral density extracted from the solvation dynamics probed by ultra-fast laser spectroscopy techniques such as the dynamic Stokes shift and three pulse photon echo spectroscopy. Our results are used to define under what conditions the dynamics of the excited chromophore is dominated by the surrounding protein and when it is dominated by dielectric fluctuations in the solvent. We show that even when the chromophore is shielded from the solvent by the protein ultra-fast solvation can be dominated by the solvent. Hence, we suggest that the ultra-fast solvation recently seen in some biological chromophores should not necessarily be assigned to ultra-fast protein dynamics. The magnitudes of the spectral density that we estimate from our continuum models and extracted from experiment suggest that most quantum dynamics of electronic excitations is incoherent. A possible exception is transfer of excitons between neigbouring chromophores in photosynthetic systems.

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“…In the recent past, many experimental studies are reported in literature on the correlated properties of water around proteins in their folded native as well as non-native states [9][10][11][12][13][14][15][16][17][18][19][20][21][22]. Ultrafast fluorescence spectroscopic studies have shown restricted environment of water at the surface of proteins with bimodal distribution of solvation times [11][12][13].…”

Section: Introductionmentioning

confidence: 99%

“…While the ultrafast component within a few picoseconds was attributed to librational and reorientational motions of the hydration water, the slower component in the range of tens of picoseconds was attributed to the restricted dynamics of water correlated with the side chain motions of the protein residues. Bhattacharyya and coworkers [16,17] have shown that the solvation dynamics of non-native states of a protein can be different than the native state depending on the location of the probe molecules. Recently, Havenith and co-workers [14,15], have shown that terahertz (THz) spectroscopy can be used as an effective tool to measure the thickness of hydration layer around proteins and the dynamics of water in it.…”

Section: Introductionmentioning

confidence: 99%

Effect of unfolding on the thickness of the hydration layer of a protein

2009

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Properties of water in the hydration layer around a protein is intimately correlated with its function. A knowledge of the thickness of the hydration layer is important to understand its role in guiding the foldingunfolding of the protein. We have performed atomistic molecular dynamics simulations of the folded native and a partially unfolded molten globule structure of the villin headpiece subdomain or HP-36 in aqueous solution to estimate the effect of unfolding on the thickness of hydration layer around different segments of the protein. In particular, several dynamic properties of water around different segments of the folded native and the unfolded structure have been calculated by varying the thickness of the hydration layers. It is found that unfolding of a segment of the protein is correlated with the dynamics of water around it, i.e., within the first hydration layer. The effect of unfolding on water properties has been found to diminish when water molecules present beyond the first hydration layer were included in the calculations.

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Solvation Dynamics in the Molten Globule State of a Protein

Cited by 49 publications

References 48 publications

Does the Dynamic Stokes Shift Report on Slow Protein Hydration Dynamics?

Does the Dynamic Stokes Shift Report on Slow Protein Hydration Dynamics?

Quantum Dynamics of Electronic Excitations in Biomolecular Chromophores: Role of the Protein Environment and Solvent

Effect of unfolding on the thickness of the hydration layer of a protein

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