Preface: Special Topic on Biological Water Gerhard Hummer and Andrei Tokmakoff Citation: The Journal of Chemical Physics 141, 22D101 (2014); doi: 10.1063/1.4901337 View online: http://dx.doi.org/10.1063/1.4901337 View Table of Contents: http://scitation.aip.org/content/aip/journal/jcp/141/22?ver=pdfcov Published by the AIP Publishing Articles you may be interested in Infrared spectral marker bands characterizing a transient water wire inside a hydrophobic membrane protein J. Chem. Phys. 141, 22D524 (2014); 10.1063/1.4902237 A statistical mechanical approach to protein aggregation J. Chem. Phys. 135, 235102 (2011); 10.1063/1.3666837 Communication maps computed for homodimeric hemoglobin: Computational study of water-mediated energy transport in proteins J. Chem. Phys. 135, 065103 (2011); 10.1063/1.3623423 Atomic decomposition of the protein solvation free energy and its application to amyloid-beta protein in water J. Chem. Phys. 135, 034506 (2011); 10.1063/1.3610550 Relationship between population of the fibril-prone conformation in the monomeric state and oligomer formation times of peptides: Insights from all-atom simulations J. Chem. Phys. 132, 165104 (2010); 10.1063/1.3415372
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THE JOURNAL OF CHEMICAL PHYSICS 141, 22D101 (2014)
Preface: Special Topic on Biological Water Gerhard Hummer1 and Andrei Tokmakoff2 1
Department of Theoretical Biophysics, Max Planck Institute of Biophysics, Max-von-Laue-Straße 3, D-60438 Frankfurt am Main, Germany 2 Department of Chemistry, The Institute for Biophysical Dynamics, and The James Franck Institute, University of Chicago, 929 E. 57th St., Chicago, Illinois 60637, USA
(Received 24 October 2014; accepted 29 October 2014; published online 13 November 2014) This special issue presents a series of papers that highlight a new and evolving view of water’s molecular role in biological structure and dynamics. Increasingly water is appreciated for playing an active role in biological function rather than just serving as a spectator. The areas represented include molecular interfaces with water, biological self-assembly, conformational changes by macromolecules, and chemical reactivity. © 2014 AIP Publishing LLC. [http://dx.doi.org/10.1063/1.4901337] The unique role of water in living systems has long been recognized. As a powerful solvent for polar substances and a poor solvent for nonpolar ones, water drives the central biological self-assembly processes of protein and nucleic acid folding, biomolecular complex formation, and lipid membrane formation. Beyond stabilizing biomolecular structures, though, the central role of water in many biological functions is increasingly appreciated, from proton conduction in biological energy conversion and the gating of ion channels in biological signal transduction to the facilitation of protein dynamics and allostery. With each passing decade new insights emerge and our understanding of the behavior of molecules in an aqueous environment becomes more nuanced. Chemical physics research on the fundamental properties of liquid water and aqueous solutions has gone hand-in-hand with studies of the biological properties of water. The result is a deeper understanding of water in living systems, as reflected in the articles of this special issue. What propels this growth of interest in biological water? Revisiting the past decade allows us to see a distinct shift of scope by the participants in this field. Most notably, there is an increasing appreciation and research capability for explicit molecular studies of water participation in processes as diverse as diffusion and transport, solvation, biomolecular interactions and conformational changes, self-assembly and hydrophobicity, proton and ion conduction, and chemical reaction dynamics. Water is no longer just a solvent modeled as a homogeneous dielectric medium. Instead, the molecular properties of water and their manifestation in unique physical and chemical characteristics occupy central roles, and water becomes an active participant in biological processes. The result is that the conceptual boundaries of what we view as “functional water” have expanded dramatically, and at the same time the physical boundaries we perceive between water and its biomolecular partners are dissolving. For instance the structure, dynamics, and physical properties of water at the boundary with proteins are intimately intertwined. These coupled properties depend in striking ways on additional partners, be they ions, solutes that have specific or nonspecific interactions with the protein, or physical constraints that crowd or confine the system. When we discuss 0021-9606/2014/141(22)/22D101/2/$30.00
molecular flexibility, folding, or binding, solvating water is often an equal partner in the description of the dynamics of these processes. Collective behavior of hydrogen bonded water molecules also features prominently in studies of hydrophobicity and dewetting, water confinement, hydrogen bond reorganization, or vibrational and electronic states. Water is also central to biological energy conversion and many biochemical reactions, not least by serving as a wire for fast Grotthuss-type proton transport. Part of this shift towards a fully molecular view of biological water results from new research capabilities that allow us to study the previously inaccessible. New experimental techniques make it possible to resolve molecular water previously masked by the bulk signal. Experimental methods in areas including ultrafast optical, infrared, and terahertz spectroscopies, electron and nuclear magnetic resonance, as well as X-ray and neutron spectroscopy and scattering continue to advance in structural and temporal resolution. The need to interpret these experiments of growing complexity has stimulated rapid developments of theoretical tools and molecular simulations to unify the physical principles. Computational methods have emerged that highlight explicit molecular structure and the connection to biomolecular processes. Even inherently quantum mechanical phenomena such as chemical dynamics are being treated more comprehensively in computational studies. These new capabilities in experiment and theory have allowed chemical physicists to shift from model systems to problems of immediate biological relevance. In the present special issue, we highlight representative— but certainly not comprehensive—studies of the role of water at a molecular level in biological structure, dynamics, and function. These reflect a number of general areas that we consider important in current and future research: (1) the physical properties of molecular interfaces between water and biomolecules from the 10−11 to the 10−8 m scale, and their influence on chemical reactivity and solubility; (2) water’s role in self-assembly of biomolecules and membranes, including aggregation and the hydrophobic effect; (3) water’s participation in large amplitude conformational changes, such as those that occur in folding, allostery, gating, or signaling; (4) water’s role mediating specific interactions between molecules,
141, 22D101-1
© 2014 AIP Publishing LLC
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22D101-2
G. Hummer and A. Tokmakoff
for instance, in recognition and binding; (5) water’s role in biological energy conversion, including catalysis, charge transport, and force generation; and (6) how water’s molecular interaction with ions governs electrical properties varying
J. Chem. Phys. 141, 22D101 (2014)
from proton transport and pKa s to the membrane potential. It is our hope that highlighting these research thrusts provides a glimpse in each of these directions and encourages others to enter and advance this field.
This article is copyrighted as indicated in the article. Reuse of AIP content is subject to the terms at: http://scitation.aip.org/termsconditions. Downloaded to IP: 129.173.72.87 On: Tue, 30 Dec 2014 15:21:42
This article is copyrighted as indicated in the article. Reuse of AIP content is subject to the terms at: http://scitation.aip.org/termsconditions. Downloaded to IP: 129.173.72.87 On: Tue, 30 Dec 2014 15:21:42
THE JOURNAL OF CHEMICAL PHYSICS 141, 22D101 (2014)
Preface: Special Topic on Biological Water Gerhard Hummer1 and Andrei Tokmakoff2 1
Department of Theoretical Biophysics, Max Planck Institute of Biophysics, Max-von-Laue-Straße 3, D-60438 Frankfurt am Main, Germany 2 Department of Chemistry, The Institute for Biophysical Dynamics, and The James Franck Institute, University of Chicago, 929 E. 57th St., Chicago, Illinois 60637, USA
(Received 24 October 2014; accepted 29 October 2014; published online 13 November 2014) This special issue presents a series of papers that highlight a new and evolving view of water’s molecular role in biological structure and dynamics. Increasingly water is appreciated for playing an active role in biological function rather than just serving as a spectator. The areas represented include molecular interfaces with water, biological self-assembly, conformational changes by macromolecules, and chemical reactivity. © 2014 AIP Publishing LLC. [http://dx.doi.org/10.1063/1.4901337] The unique role of water in living systems has long been recognized. As a powerful solvent for polar substances and a poor solvent for nonpolar ones, water drives the central biological self-assembly processes of protein and nucleic acid folding, biomolecular complex formation, and lipid membrane formation. Beyond stabilizing biomolecular structures, though, the central role of water in many biological functions is increasingly appreciated, from proton conduction in biological energy conversion and the gating of ion channels in biological signal transduction to the facilitation of protein dynamics and allostery. With each passing decade new insights emerge and our understanding of the behavior of molecules in an aqueous environment becomes more nuanced. Chemical physics research on the fundamental properties of liquid water and aqueous solutions has gone hand-in-hand with studies of the biological properties of water. The result is a deeper understanding of water in living systems, as reflected in the articles of this special issue. What propels this growth of interest in biological water? Revisiting the past decade allows us to see a distinct shift of scope by the participants in this field. Most notably, there is an increasing appreciation and research capability for explicit molecular studies of water participation in processes as diverse as diffusion and transport, solvation, biomolecular interactions and conformational changes, self-assembly and hydrophobicity, proton and ion conduction, and chemical reaction dynamics. Water is no longer just a solvent modeled as a homogeneous dielectric medium. Instead, the molecular properties of water and their manifestation in unique physical and chemical characteristics occupy central roles, and water becomes an active participant in biological processes. The result is that the conceptual boundaries of what we view as “functional water” have expanded dramatically, and at the same time the physical boundaries we perceive between water and its biomolecular partners are dissolving. For instance the structure, dynamics, and physical properties of water at the boundary with proteins are intimately intertwined. These coupled properties depend in striking ways on additional partners, be they ions, solutes that have specific or nonspecific interactions with the protein, or physical constraints that crowd or confine the system. When we discuss 0021-9606/2014/141(22)/22D101/2/$30.00
molecular flexibility, folding, or binding, solvating water is often an equal partner in the description of the dynamics of these processes. Collective behavior of hydrogen bonded water molecules also features prominently in studies of hydrophobicity and dewetting, water confinement, hydrogen bond reorganization, or vibrational and electronic states. Water is also central to biological energy conversion and many biochemical reactions, not least by serving as a wire for fast Grotthuss-type proton transport. Part of this shift towards a fully molecular view of biological water results from new research capabilities that allow us to study the previously inaccessible. New experimental techniques make it possible to resolve molecular water previously masked by the bulk signal. Experimental methods in areas including ultrafast optical, infrared, and terahertz spectroscopies, electron and nuclear magnetic resonance, as well as X-ray and neutron spectroscopy and scattering continue to advance in structural and temporal resolution. The need to interpret these experiments of growing complexity has stimulated rapid developments of theoretical tools and molecular simulations to unify the physical principles. Computational methods have emerged that highlight explicit molecular structure and the connection to biomolecular processes. Even inherently quantum mechanical phenomena such as chemical dynamics are being treated more comprehensively in computational studies. These new capabilities in experiment and theory have allowed chemical physicists to shift from model systems to problems of immediate biological relevance. In the present special issue, we highlight representative— but certainly not comprehensive—studies of the role of water at a molecular level in biological structure, dynamics, and function. These reflect a number of general areas that we consider important in current and future research: (1) the physical properties of molecular interfaces between water and biomolecules from the 10−11 to the 10−8 m scale, and their influence on chemical reactivity and solubility; (2) water’s role in self-assembly of biomolecules and membranes, including aggregation and the hydrophobic effect; (3) water’s participation in large amplitude conformational changes, such as those that occur in folding, allostery, gating, or signaling; (4) water’s role mediating specific interactions between molecules,
141, 22D101-1
© 2014 AIP Publishing LLC
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22D101-2
G. Hummer and A. Tokmakoff
for instance, in recognition and binding; (5) water’s role in biological energy conversion, including catalysis, charge transport, and force generation; and (6) how water’s molecular interaction with ions governs electrical properties varying
J. Chem. Phys. 141, 22D101 (2014)
from proton transport and pKa s to the membrane potential. It is our hope that highlighting these research thrusts provides a glimpse in each of these directions and encourages others to enter and advance this field.
This article is copyrighted as indicated in the article. Reuse of AIP content is subject to the terms at: http://scitation.aip.org/termsconditions. Downloaded to IP: 129.173.72.87 On: Tue, 30 Dec 2014 15:21:42
