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Title: Ice-nucleating bacteria control the order and dynamics of interfacial water

Abstract

Ice-nucleating organisms play important roles in the environment. With their ability to induce ice formation at temperatures just below the ice melting point, bacteria such as Pseudomonas syringae attack plants through frost damage using specialized ice-nucleating proteins. Besides the impact on agriculture and microbial ecology, airborne P. syringae can affect atmospheric glaciation processes, with consequences for cloud evolution, precipitation, and climate. Biogenic ice nucleation is also relevant for artificial snow production and for biomimetic materials for controlled interfacial freezing. We use interface-specific sum frequency generation (SFG) spectroscopy to show that hydrogen bonding at the water-bacteria contact imposes structural ordering on the adjacent water network. Experimental SFG data and molecular dynamics simulations demonstrate that ice active sites within P. syringae feature unique hydrophilic-hydrophobic patterns to enhance ice nucleation. Finally, the freezing transition is further facilitated by the highly effective removal of latent heat from the nucleation site, as apparent from time-resolved SFG spectroscopy.

Authors:
 [1];  [2];  [3];  [4];  [4];  [2];  [2];  [5];  [2];  [2];  [5];  [6];  [5];  [2];  [7]
+ Show Author Affiliations
  1. Max Planck Institute for Polymer Research, Mainz (Germany); Univ. of Texas, Austin, TX (United States)
  2. Max Planck Institute for Polymer Research, Mainz (Germany)
  3. Max Planck Institute for Polymer Research, Mainz (Germany); Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
  4. Univ. of Washington, Seattle, WA (United States)
  5. Max Planck Institute for Chemistry, Mainz (Germany)
  6. Stony Brook Univ., Stony Brook, NY (United States)
  7. Max Planck Institute for Polymer Research, Mainz (Germany); Univ. of Washington, Seattle, WA (United States)
Publication Date:
Research Org.:
Stony Brook Univ., NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1349437
Grant/Contract Number:  
SC0008613
Resource Type:
Accepted Manuscript
Journal Name:
Science Advances
Additional Journal Information:
Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2375-2548
Publisher:
AAAS
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; ice nucleation; Pseudomonas Syringae; ice protein; sum frequency generation

Citation Formats

Pandey, Ravindra, Usui, Kota, Livingstone, Ruth A., Fischer, Sean A., Pfaendtner, Jim, Backus, Ellen H. G., Nagata, Yuki, Frohlich-Nowoisky, Janine, Schmuser, Lars, Mauri, Sergio, Scheel, Jan F., Knopf, Daniel A., Poschl, Ulrich, Bonn, Mischa, and Weidner, Tobias. Ice-nucleating bacteria control the order and dynamics of interfacial water. United States: N. p., 2016. Web. doi:10.1126/sciadv.1501630.
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Pandey, Ravindra, Usui, Kota, Livingstone, Ruth A., Fischer, Sean A., Pfaendtner, Jim, Backus, Ellen H. G., Nagata, Yuki, Frohlich-Nowoisky, Janine, Schmuser, Lars, Mauri, Sergio, Scheel, Jan F., Knopf, Daniel A., Poschl, Ulrich, Bonn, Mischa, & Weidner, Tobias. Ice-nucleating bacteria control the order and dynamics of interfacial water. United States. https://doi.org/10.1126/sciadv.1501630
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Pandey, Ravindra, Usui, Kota, Livingstone, Ruth A., Fischer, Sean A., Pfaendtner, Jim, Backus, Ellen H. G., Nagata, Yuki, Frohlich-Nowoisky, Janine, Schmuser, Lars, Mauri, Sergio, Scheel, Jan F., Knopf, Daniel A., Poschl, Ulrich, Bonn, Mischa, and Weidner, Tobias. Fri . "Ice-nucleating bacteria control the order and dynamics of interfacial water". United States. https://doi.org/10.1126/sciadv.1501630. https://www.osti.gov/servlets/purl/1349437.
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@article{osti_1349437,
title = {Ice-nucleating bacteria control the order and dynamics of interfacial water},
author = {Pandey, Ravindra and Usui, Kota and Livingstone, Ruth A. and Fischer, Sean A. and Pfaendtner, Jim and Backus, Ellen H. G. and Nagata, Yuki and Frohlich-Nowoisky, Janine and Schmuser, Lars and Mauri, Sergio and Scheel, Jan F. and Knopf, Daniel A. and Poschl, Ulrich and Bonn, Mischa and Weidner, Tobias},
abstractNote = {Ice-nucleating organisms play important roles in the environment. With their ability to induce ice formation at temperatures just below the ice melting point, bacteria such as Pseudomonas syringae attack plants through frost damage using specialized ice-nucleating proteins. Besides the impact on agriculture and microbial ecology, airborne P. syringae can affect atmospheric glaciation processes, with consequences for cloud evolution, precipitation, and climate. Biogenic ice nucleation is also relevant for artificial snow production and for biomimetic materials for controlled interfacial freezing. We use interface-specific sum frequency generation (SFG) spectroscopy to show that hydrogen bonding at the water-bacteria contact imposes structural ordering on the adjacent water network. Experimental SFG data and molecular dynamics simulations demonstrate that ice active sites within P. syringae feature unique hydrophilic-hydrophobic patterns to enhance ice nucleation. Finally, the freezing transition is further facilitated by the highly effective removal of latent heat from the nucleation site, as apparent from time-resolved SFG spectroscopy.},
doi = {10.1126/sciadv.1501630},
journal = {Science Advances},
number = 4,
volume = 2,
place = {United States},
year = {Fri Apr 22 00:00:00 EDT 2016},
month = {Fri Apr 22 00:00:00 EDT 2016}
}
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https://doi.org/10.1126/sciadv.1501630
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Ubiquity of Biological Ice Nucleators in Snowfall
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Comparative study of hydration shell dynamics around a hyperactive antifreeze protein and around ubiquitin
journal, December 2014

  • Duboué-Dijon, Elise; Laage, Damien
  • The Journal of Chemical Physics, Vol. 141, Issue 22
  • DOI: 10.1063/1.4902822

A peek at ice binding by antifreeze proteins
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Liquid flow along a solid surface reversibly alters interfacial chemistry
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Protein interaction with ice
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Resonant intermolecular transfer of vibrational energy in liquid water
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Molecular dynamics simulation of quasi-two-dimensional water clusters on ice nucleation protein
journal, August 2012

  • Murakami, Daisuke; Yasuoka, Kenji
  • The Journal of Chemical Physics, Vol. 137, Issue 5
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Hydrogen bonding and Raman, IR, and 2D-IR spectroscopy of dilute HOD in liquid D2O
journal, June 2007

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  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 36
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On the orientational relaxation of HDO in liquid water
journal, September 2005

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  • The Journal of Chemical Physics, Vol. 123, Issue 11
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Homogeneous Bulk, Surface, and Edge Nucleation in Crystalline Nanodroplets
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The effects of steric mutations on the structure of type III antifreeze protein and its interaction with ice
journal, January 1998

  • DeLuca, Carl I.; Davies, Peter L.; Ye, Qilu
  • Journal of Molecular Biology, Vol. 275, Issue 3
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Climate Change 2013 – The Physical Science Basis
book, March 2014

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    • Sayer, Thomas; Cox, Stephen
    • Apollo - University of Cambridge Repository
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