Preferential Ordering and Organization of Hydration Water Favor Nucleation of Ice by Ice-Nucleating Proteins over Antifreeze Proteins.

Bacteria containing ice-nucleating proteins (INPs) evolved in nature to nucleate ice at the high sub-zero ambiance. The ability of the INPs to induce order in the hydration layer and their aggregation propensity appear to be key factors of their ice nucleation abilities. However, the mechanism of the process of ice nucleation by INPs is yet to be understood clearly. Here, we have performed all-atom molecular dynamics simulations and analyzed the structure and dynamics of the hydration layer around the proposed ice-nucleating surface of a model INP. Results are compared with the hydration of a topologically similar non-ice-binding protein (non-IBP) and another ice-growth inhibitory antifreeze protein (sbwAFP). We observed that the hydration structure around the ice-nucleating surface of INP is highly ordered and the dynamics of the hydration water are slower, compared to the non-IBP. Even the ordering of the hydration layer is more evident around the ice-binding surface of INP, compared to the antifreeze protein sbwAFP. Particularly with increasing repeat units of INP, we observe an increased population of ice-like water. Interestingly, the distances between the hydroxyl groups of the threonine ladder and its associated channel water of the ice-binding surface (IBS) of INP in the X and Y direction mimic the oxygen atom distances of the basal plane of hexagonal ice. However, the structural synergies between the hydroxyl group distances of the threonine ladder and its associated channel water of the IBS of sbwAFP and oxygen atom distances of the basal plane are less evident. This difference makes the IBS of the INP a better template for ice nucleation than AFP, although both of them bind to the ice surface efficiently.

[1]  S. Bandyopadhyay,et al.  Elucidating the Sluggish Water Dynamics at the Ice-Binding Surface of the Hyperactive Tenebrio molitor Antifreeze Protein. , 2023, The journal of physical chemistry. B.

[2]  Sandip Chakraborty,et al.  Number of Hydrogen Bonds per Unit Solvent Accessible Surface Area: A Descriptor of Functional States of Proteins. , 2022, The journal of physical chemistry. B.

[3]  Sandip Chakraborty,et al.  Molecular Factors of Ice Growth Inhibition for Hyperactive and Globular Antifreeze Proteins: Insights from Molecular Dynamics Simulation. , 2022, Langmuir : the ACS journal of surfaces and colloids.

[4]  Y. Rudich,et al.  Water-organizing motif continuity is critical for potent ice nucleation protein activity , 2022, Nature Communications.

[5]  Sandip Chakraborty,et al.  Decoding molecular factors shaping human angiotensin converting enzyme 2 receptor usage by spike glycoprotein in lineage B beta-coronaviruses , 2022, Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease.

[6]  M. Bonn,et al.  Toward Understanding Bacterial Ice Nucleation , 2022, The journal of physical chemistry. B.

[7]  T. Weidner,et al.  Electrostatics Trigger Interfacial Self-Assembly of Bacterial Ice Nucleators. , 2021, Biomacromolecules.

[8]  B. Jana,et al.  Differential Hydration of Ice‐Binding Surface of Globular and Hyperactive Antifreeze Proteins , 2021, Advanced Theory and Simulations.

[9]  J. Pfaendtner,et al.  Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water , 2021, Nature Communications.

[10]  Katrin F. Domke,et al.  Specific Ion–Protein Interactions Influence Bacterial Ice Nucleation , 2021, Chemistry.

[11]  M. Bonn,et al.  Interfacial Water Ordering Is Insufficient to Explain Ice-Nucleating Protein Activity. , 2020, The journal of physical chemistry letters.

[12]  M. Bonn,et al.  Inhibition of Bacterial Ice Nucleators is Not an Intrinsic Property of Antifreeze Proteins. , 2020, The journal of physical chemistry. B.

[13]  B. Jana,et al.  Deciphering the Role of Non-Ice-Binding Surface on the Antifreeze Activity of Hyperactive Antifreeze Proteins. , 2020, The journal of physical chemistry. B.

[14]  U. Pöschl,et al.  Electrostatic Interactions Control the Functionality of Bacterial Ice Nucleators. , 2020, Journal of the American Chemical Society.

[15]  B. Jana,et al.  Calcium ion implicitly modulates the adsorption ability of ion-dependent type II antifreeze proteins on an ice/water interface: a structural insight. , 2019, Metallomics : integrated biometal science.

[16]  Jakub Rydzewski,et al.  Promoting transparency and reproducibility in enhanced molecular simulations , 2019, Nature Methods.

[17]  V. Molinero,et al.  Hydrogen-Bonding and Hydrophobic Groups Contribute Equally to the Binding of Hyperactive Antifreeze and Ice-Nucleating Proteins to Ice. , 2019, Journal of the American Chemical Society.

[18]  B. Jana,et al.  Factors Promoting the Formation of Clathrate-Like Ordering of Water in Biomolecular Structure at Ambient Temperature and Pressure. , 2019, The journal of physical chemistry. B.

[19]  V. Molinero,et al.  How Size and Aggregation of Ice-Binding Proteins Control Their Ice Nucleation Efficiency. , 2018, Journal of the American Chemical Society.

[20]  B. Jana,et al.  Molecular Insights into the Unusual Structure of an Antifreeze Protein with a Hydrated Core. , 2018, The journal of physical chemistry. B.

[21]  F. Paesani,et al.  Ice-Nucleating and Antifreeze Proteins Recognize Ice through a Diversity of Anchored Clathrate and Ice-like Motifs. , 2018, Journal of the American Chemical Society.

[22]  B. Jana,et al.  Optimum Number of Anchored Clathrate Water and Its Instantaneous Fluctuations Dictate Ice Plane Recognition Specificities of Insect Antifreeze Protein. , 2018, The journal of physical chemistry. B.

[23]  P. Field,et al.  Strong control of Southern Ocean cloud reflectivity by ice-nucleating particles , 2018, Proceedings of the National Academy of Sciences.

[24]  D. Schmale,et al.  Ice nucleation active bacteria in precipitation are genetically diverse and nucleate ice by employing different mechanisms , 2017, The ISME Journal.

[25]  B. Jana,et al.  Molecular Insight into the Adsorption of Spruce Budworm Antifreeze Protein to an Ice Surface: A Clathrate-Mediated Recognition Mechanism. , 2017, Langmuir : the ACS journal of surfaces and colloids.

[26]  M. Bonn,et al.  Ice-nucleating bacteria control the order and dynamics of interfacial water , 2016, Science Advances.

[27]  Feng-Hsu Lin,et al.  An Antifreeze Protein Folds with an Interior Network of More Than 400 Semi-Clathrate Waters , 2014, Science.

[28]  U. Pöschl,et al.  Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere , 2014, Global change biology.

[29]  S. Sherwood,et al.  Climate Effects of Aerosol-Cloud Interactions , 2014, Science.

[30]  Massimiliano Bonomi,et al.  PLUMED 2: New feathers for an old bird , 2013, Comput. Phys. Commun..

[31]  Konrad Meister,et al.  Long-range protein–water dynamics in hyperactive insect antifreeze proteins , 2012, Proceedings of the National Academy of Sciences.

[32]  B. Murray,et al.  Ice nucleation by particles immersed in supercooled cloud droplets. , 2012, Chemical Society reviews.

[33]  J. Doye,et al.  Local order parameters for use in driving homogeneous ice nucleation with all-atom models of water. , 2012, The Journal of chemical physics.

[34]  K. Yasuoka,et al.  Molecular dynamics simulation of quasi-two-dimensional water clusters on ice nucleation protein. , 2012, The Journal of chemical physics.

[35]  R. Campbell,et al.  Novel dimeric β-helical model of an ice nucleation protein with bridged active sites , 2011, BMC Structural Biology.

[36]  Enge Wang,et al.  Melting the ice: on the relation between melting temperature and size for nanoscale ice crystals. , 2011, ACS nano.

[37]  Robert L Campbell,et al.  Anchored clathrate waters bind antifreeze proteins to ice , 2011, Proceedings of the National Academy of Sciences.

[38]  Fabio Sterpone,et al.  Reorientation and allied dynamics in water and aqueous solutions. , 2011, Annual review of physical chemistry.

[39]  U. Pöschl,et al.  Rainforest Aerosols as Biogenic Nuclei of Clouds and Precipitation in the Amazon , 2010, Science.

[40]  E. Murray,et al.  Kinetics of the homogeneous freezing of water. , 2010, Physical chemistry chemical physics : PCCP.

[41]  R. Dror,et al.  Improved side-chain torsion potentials for the Amber ff99SB protein force field , 2010, Proteins.

[42]  Zhongqin Wu,et al.  Characterization and recombinant expression of a divergent ice nucleation protein from 'Pseudomonas borealis'. , 2009, Microbiology.

[43]  Massimiliano Bonomi,et al.  PLUMED: A portable plugin for free-energy calculations with molecular dynamics , 2009, Comput. Phys. Commun..

[44]  K. Kawano,et al.  A circular loop of the 16-residue repeating unit in ice nucleation protein. , 2008, Biochemical and biophysical research communications.

[45]  David C. Sands,et al.  Ubiquity of Biological Ice Nucleators in Snowfall , 2008, Science.

[46]  M. Parrinello,et al.  Canonical sampling through velocity rescaling. , 2007, The Journal of chemical physics.

[47]  V. Hornak,et al.  Comparison of multiple Amber force fields and development of improved protein backbone parameters , 2006, Proteins.

[48]  Gerrit Groenhof,et al.  GROMACS: Fast, flexible, and free , 2005, J. Comput. Chem..

[49]  Biman Bagchi,et al.  Water dynamics in the hydration layer around proteins and micelles. , 2005, Chemical reviews.

[50]  Anthony Maxwell,et al.  A Fluoroquinolone Resistance Protein from Mycobacterium tuberculosis That Mimics DNA , 2005, Science.

[51]  U.-B. Ramløy.  Aspects of natural cold tolerance in ectothermic animals , 2000 .

[52]  Zongchao Jia,et al.  Mimicry of ice structure by surface hydroxyls and water of a β-helix antifreeze protein , 2000, Nature.

[53]  Michael J. Kuiper,et al.  β-Helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect , 2000, Nature.

[54]  Michael W. Mahoney,et al.  A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions , 2000 .

[55]  P. Rodger,et al.  Simulations of the methane hydrate/methane gas interface near hydrate forming conditions conditions , 1996 .

[56]  P. Tavan,et al.  Ligand Binding: Molecular Mechanics Calculation of the Streptavidin-Biotin Rupture Force , 1996, Science.

[57]  S. Lindow,et al.  A model of the three-dimensional structure of ice nucleation proteins. , 1993, Journal of molecular biology.

[58]  L. Kozloff,et al.  Three separate classes of bacterial ice nucleation structures , 1990, Journal of bacteriology.

[59]  G. Warren,et al.  The consensus sequence of ice nucleation proteins from Erwinia herbicola, Pseudomonas fluorescens and Pseudomonas syringae. , 1989, Gene.

[60]  S. Arai,et al.  An ice nucleation active gene of Erwinia ananas , 1989, FEBS letters.

[61]  R. Sharon,et al.  Accurate simulation of protein dynamics in solution. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[62]  S. Lindow,et al.  Size of bacterial ice-nucleation sites measured in situ by radiation inactivation analysis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[63]  P. Wolber,et al.  Conserved repeats in diverged ice nucleation structural genes from two species of Pseudomonas. , 1986, Nucleic acids research.

[64]  R. Green,et al.  Physical and functional repetition in a bacterial ice nucleation gene , 1985, Nature.

[65]  H. Berendsen,et al.  Molecular dynamics with coupling to an external bath , 1984 .

[66]  S. Nosé.  A molecular dynamics method for simulations in the canonical ensemble , 1984 .

[67]  L. Kozloff,et al.  Ice nucleating activity of Pseudomonas syringae and Erwinia herbicola , 1983, Journal of bacteriology.

[68]  S. Lindow,et al.  Bacterial ice nucleation: a factor in frost injury to plants. , 1982, Plant physiology.

[69]  F. Stillinger.  Water Revisited , 1980, Science.

[70]  L R Maki,et al.  Ice Nucleation Induced by Pseudomonas syringae , 1974, Applied microbiology.

[71]  P. Mazur.  Cryobiology: the freezing of biological systems. , 1970, Science.

[72]  T. Schlick.  Molecular Modeling and Simulation: An Interdisciplinary Guide , 2003 .

[73]  J. Duman,et al.  Antifreeze and ice nucleator proteins in terrestrial arthropods. , 2001, Annual review of physiology.

[74]  D. Chandler,et al.  Hydrogen-bond kinetics in liquid water , 1996, Nature.

[75]  E. Baker,et al.  Hydrogen bonding in globular proteins. , 1984, Progress in biophysics and molecular biology.

[76]  D. Rapaport.  Density fluctuations and hydrogen bonding in supercooled water , 1983 .