skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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]
  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., Stony Brook, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
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.
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. doi:10.1126/sciadv.1501630.
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. doi:10.1126/sciadv.1501630. https://www.osti.gov/servlets/purl/1349437.
@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 = {2016},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 53 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Bacterial Ice Nucleation: A Factor in Frost Injury to Plants
journal, October 1982

  • Lindow, Steven E.; Arny, Deane C.; Upper, Christen D.
  • Plant Physiology, Vol. 70, Issue 4
  • DOI: 10.1104/pp.70.4.1084

Molecular aspects of microbial ice nucleation
journal, February 1991


Ubiquity of Biological Ice Nucleators in Snowfall
journal, February 2008


High concentrations of biological aerosol particles and ice nuclei during and after rain
journal, January 2013

  • Huffman, J. A.; Prenni, A. J.; DeMott, P. J.
  • Atmospheric Chemistry and Physics, Vol. 13, Issue 13
  • DOI: 10.5194/acp-13-6151-2013

Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere
journal, November 2013

  • Morris, Cindy E.; Conen, Franz; Alex Huffman, J.
  • Global Change Biology, Vol. 20, Issue 2
  • DOI: 10.1111/gcb.12447

Rainforest Aerosols as Biogenic Nuclei of Clouds and Precipitation in the Amazon
journal, September 2010


Climate Effects of Aerosol-Cloud Interactions
journal, January 2014


Microbiome of the upper troposphere: Species composition and prevalence, effects of tropical storms, and atmospheric implications
journal, January 2013

  • DeLeon-Rodriguez, N.; Lathem, T. L.; Rodriguez-R, L. M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 7
  • DOI: 10.1073/pnas.1212089110

Heterogeneous ice nucleation on atmospheric aerosols: a review of results from laboratory experiments
journal, January 2012


Components of ice nucleation structures of bacteria.
journal, October 1991


A Model of the Three-dimensional Structure of Ice Nucleation Proteins
journal, August 1993

  • Kajava, Andrey V.; Lindow, Steven E.
  • Journal of Molecular Biology, Vol. 232, Issue 3
  • DOI: 10.1006/jmbi.1993.1424

Re-Evaluation of a Bacterial Antifreeze Protein as an Adhesin with Ice-Binding Activity
journal, November 2012


Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth
journal, November 2014


Novel dimeric β-helical model of an ice nucleation protein with bridged active sites
journal, January 2011

  • Garnham, Christopher P.; Campbell, Robert L.; Walker, Virginia K.
  • BMC Structural Biology, Vol. 11, Issue 1
  • DOI: 10.1186/1472-6807-11-36

Protein interaction with ice
journal, January 1992


Modeling Pseudomonas syringae Ice-Nucleation Protein as aβ-Helical Protein
journal, March 2001


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
  • DOI: 10.1063/1.4739299

Anchored clathrate waters bind antifreeze proteins to ice
journal, April 2011

  • Garnham, C. P.; Campbell, R. L.; Davies, P. L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
  • DOI: 10.1073/pnas.1100429108

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
  • DOI: 10.1006/jmbi.1997.1482

Surface Vibrational Spectroscopic Studies of Hydrogen Bonding and Hydrophobicity
journal, May 1994


Membrane-Bound Water is Energetically Decoupled from Nearby Bulk Water:  An Ultrafast Surface-Specific Investigation
journal, August 2007

  • Ghosh, Avishek; Smits, Marc; Bredenbeck, Jens
  • Journal of the American Chemical Society, Vol. 129, Issue 31
  • DOI: 10.1021/ja073130h

Liquid flow along a solid surface reversibly alters interfacial chemistry
journal, June 2014


Observation of ice-like water layers at an aqueous protein surface
journal, December 2014

  • Meister, Konrad; Strazdaite, Simona; DeVries, Arthur L.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
  • DOI: 10.1073/pnas.1414188111

BINARY: an optical freezing array for assessing temperature and time dependence of heterogeneous ice nucleation
journal, January 2015


Parameterizations for ice nucleation in biological and atmospheric systems
journal, January 2009

  • Koop, Thomas; Zobrist, Bernhard
  • Physical Chemistry Chemical Physics, Vol. 11, Issue 46
  • DOI: 10.1039/b914289d

Interfacial Water Structure Associated with Phospholipid Membranes Studied by Phase-Sensitive Vibrational Sum Frequency Generation Spectroscopy
journal, August 2010

  • Chen, Xiangke; Hua, Wei; Huang, Zishuai
  • Journal of the American Chemical Society, Vol. 132, Issue 32
  • DOI: 10.1021/ja1048237

Structure and Orientation of Water at Charged Lipid Monolayer/Water Interfaces Probed by Heterodyne-Detected Vibrational Sum Frequency Generation Spectroscopy
journal, August 2010

  • Mondal, Jahur A.; Nihonyanagi, Satoshi; Yamaguchi, Shoichi
  • Journal of the American Chemical Society, Vol. 132, Issue 31
  • DOI: 10.1021/ja104327t

Sum Frequency Generation Vibrational Spectroscopy Studies on Protein Adsorption
journal, November 2002

  • Wang, Jie; Buck, Sarah M.; Chen, Zhan
  • The Journal of Physical Chemistry B, Vol. 106, Issue 44
  • DOI: 10.1021/jp021363j

Observation of buried water molecules in phospholipid membranes by surface sum-frequency generation spectroscopy
journal, October 2009

  • Sovago, Maria; Vartiainen, Erik; Bonn, Mischa
  • The Journal of Chemical Physics, Vol. 131, Issue 16
  • DOI: 10.1063/1.3257600

Ice nucleation by particles immersed in supercooled cloud droplets
journal, January 2012

  • Murray, B. J.; O'Sullivan, D.; Atkinson, J. D.
  • Chemical Society Reviews, Vol. 41, Issue 19
  • DOI: 10.1039/c2cs35200a

Homogeneous Ice Nucleation From Aqueous Inorganic/Organic Particles Representative of Biomass Burning: Water Activity, Freezing Temperatures, Nucleation Rates
journal, February 2011

  • Knopf, Daniel A.; Rigg, Yannick J.
  • The Journal of Physical Chemistry A, Vol. 115, Issue 5
  • DOI: 10.1021/jp109171g

A water activity based model of heterogeneous ice nucleation kinetics for freezing of water and aqueous solution droplets
journal, January 2013

  • Knopf, Daniel A.; Alpert, Peter A.
  • Faraday Discussions, Vol. 165
  • DOI: 10.1039/c3fd00035d

Theoretical vibrational sum-frequency generation spectroscopy of water near lipid and surfactant monolayer interfaces
journal, November 2014

  • Roy, S.; Gruenbaum, S. M.; Skinner, J. L.
  • The Journal of Chemical Physics, Vol. 141, Issue 18
  • DOI: 10.1063/1.4895546

Surface of Liquid Water: Three-Body Interactions and Vibrational Sum-Frequency Spectroscopy
journal, July 2011

  • Pieniazek, Piotr A.; Tainter, Craig J.; Skinner, James L.
  • Journal of the American Chemical Society, Vol. 133, Issue 27
  • DOI: 10.1021/ja2026695

Investigation of the Ice-Binding Site of an Insect Antifreeze Protein Using Sum-Frequency Generation Spectroscopy
journal, March 2015

  • Meister, Konrad; Lotze, Stephan; Olijve, Luuk L. C.
  • The Journal of Physical Chemistry Letters, Vol. 6, Issue 7
  • DOI: 10.1021/acs.jpclett.5b00281

Bio-Inspired Strategies for Anti-Icing
journal, March 2014

  • Lv, Jianyong; Song, Yanlin; Jiang, Lei
  • ACS Nano, Vol. 8, Issue 4
  • DOI: 10.1021/nn406522n

The molecular structure of the interface between water and a hydrophobic substrate is liquid-vapor like
journal, November 2014

  • Willard, Adam P.; Chandler, David
  • The Journal of Chemical Physics, Vol. 141, Issue 18
  • DOI: 10.1063/1.4897249

Thermodynamics of Heterogeneous Crystal Nucleation in Contact and Immersion Modes
journal, November 2008

  • Djikaev, Y. S.; Ruckenstein, E.
  • The Journal of Physical Chemistry A, Vol. 112, Issue 46
  • DOI: 10.1021/jp803155f

Fast Imaging of Freezing Drops: No Preference for Nucleation at the Contact Line
journal, May 2011

  • Gurganus, Colin; Kostinski, Alexander B.; Shaw, Raymond A.
  • The Journal of Physical Chemistry Letters, Vol. 2, Issue 12
  • DOI: 10.1021/jz2004528

Evaporation freezing by contact nucleation inside-out
journal, January 2005


Heterogeneous Surface Crystallization Observed in Undercooled Water
journal, May 2005

  • Shaw, Raymond A.; Durant, Adam J.; Mi, Youshi
  • The Journal of Physical Chemistry B, Vol. 109, Issue 20
  • DOI: 10.1021/jp0506336

Nucleation at the Contact Line Observed on Nanotextured Surfaces
journal, December 2014


Ice nucleation behaviour on sol–gel coatings with different surface energy and roughness
journal, January 2015

  • Fu, Q. T.; Liu, E. J.; Wilson, P.
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 33
  • DOI: 10.1039/C5CP03243A

Homogeneous Bulk, Surface, and Edge Nucleation in Crystalline Nanodroplets
journal, December 2010


Ice Nucleation by Alcohols Arranged in Monolayers at the Surface of Water Drops
journal, November 1990


Heterogeneous Nucleation of Ice on Carbon Surfaces
journal, February 2014

  • Lupi, Laura; Hudait, Arpa; Molinero, Valeria
  • Journal of the American Chemical Society, Vol. 136, Issue 8
  • DOI: 10.1021/ja411507a

Extreme surface propensity of halide ions in water
journal, June 2014

  • Piatkowski, Lukasz; Zhang, Zhen; Backus, Ellen H. G.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5083

Resonant intermolecular transfer of vibrational energy in liquid water
journal, December 1999

  • Woutersen, Sander; Bakker, Huib J.
  • Nature, Vol. 402, Issue 6761
  • DOI: 10.1038/990058

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

Nuclear Quantum Effects Affect Bond Orientation of Water at the Water-Vapor Interface
journal, November 2012


Orientational dynamics of isotopically diluted H2O and D2O
journal, October 2006

  • Rezus, Y. L. A.; Bakker, H. J.
  • The Journal of Chemical Physics, Vol. 125, Issue 14
  • DOI: 10.1063/1.2353831

Temperature dependence of the surface tension of water by the equilibrium ring method
journal, November 1972

  • Cini, Renato; Loglio, Giuseppe; Ficalbi, Augusta
  • Journal of Colloid and Interface Science, Vol. 41, Issue 2
  • DOI: 10.1016/0021-9797(72)90113-0

Specific Ion Effects at the Air/Water Interface
journal, April 2006

  • Jungwirth, Pavel; Tobias, Douglas J.
  • Chemical Reviews, Vol. 106, Issue 4
  • DOI: 10.1021/cr0403741

Covalent Immobilization of Antibody Fragments onto Langmuir−Schaefer Binary Monolayers Chemisorbed on Gold
journal, June 2002


GROMACS 4:  Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation
journal, February 2008

  • Hess, Berk; Kutzner, Carsten; van der Spoel, David
  • Journal of Chemical Theory and Computation, Vol. 4, Issue 3
  • DOI: 10.1021/ct700301q

The melting temperature of the most common models of water
journal, March 2005

  • Vega, C.; Sanz, E.; Abascal, J. L. F.
  • The Journal of Chemical Physics, Vol. 122, Issue 11
  • DOI: 10.1063/1.1862245

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993

  • Darden, Tom; York, Darrin; Pedersen, Lee
  • The Journal of Chemical Physics, Vol. 98, Issue 12
  • DOI: 10.1063/1.464397

Canonical sampling through velocity rescaling
journal, January 2007

  • Bussi, Giovanni; Donadio, Davide; Parrinello, Michele
  • The Journal of Chemical Physics, Vol. 126, Issue 1
  • DOI: 10.1063/1.2408420

Hydrogen bonding and Raman, IR, and 2D-IR spectroscopy of dilute HOD in liquid D2O
journal, June 2007

  • Auer, B.; Kumar, R.; Schmidt, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 36
  • DOI: 10.1073/pnas.0701482104

Infrared and Raman line shapes for ice Ih. I. Dilute HOD in H2O and D2O
journal, May 2010

  • Li, F.; Skinner, J. L.
  • The Journal of Chemical Physics, Vol. 132, Issue 20
  • DOI: 10.1063/1.3430518

Interpretation of the water surface vibrational sum-frequency spectrum
journal, July 2011

  • Pieniazek, P. A.; Tainter, C. J.; Skinner, J. L.
  • The Journal of Chemical Physics, Vol. 135, Issue 4
  • DOI: 10.1063/1.3613623

Structural Inhomogeneity of Interfacial Water at Lipid Monolayers Revealed by Surface-Specific Vibrational Pump−Probe Spectroscopy
journal, October 2010

  • Bonn, Mischa; Bakker, Huib J.; Ghosh, Avishek
  • Journal of the American Chemical Society, Vol. 132, Issue 42
  • DOI: 10.1021/ja106194u

Ultrafast intermolecular energy transfer in heavy water
journal, January 2009

  • Piatkowski, L.; Eisenthal, K. B.; Bakker, H. J.
  • Physical Chemistry Chemical Physics, Vol. 11, Issue 40
  • DOI: 10.1039/b908975f

On the orientational relaxation of HDO in liquid water
journal, September 2005

  • Rezus, Y. L. A.; Bakker, H. J.
  • The Journal of Chemical Physics, Vol. 123, Issue 11
  • DOI: 10.1063/1.2009729

    Works referencing / citing this record:

    Stabilization of AgI's polar surfaces by the aqueous environment, and its implications for ice formation
    journal, January 2019

    • Sayer, Thomas; Cox, Stephen J.
    • Physical Chemistry Chemical Physics, Vol. 21, Issue 27
    • DOI: 10.1039/c9cp02193k

    Nanomaterial–microbe cross-talk: physicochemical principles and (patho)biological consequences
    journal, January 2018

    • Westmeier, D.; Hahlbrock, A.; Reinhardt, C.
    • Chemical Society Reviews, Vol. 47, Issue 14
    • DOI: 10.1039/c6cs00691d

    Refreeze experiments with water droplets containing different types of ice nuclei interpreted by classical nucleation theory
    journal, January 2017

    • Kaufmann, Lukas; Marcolli, Claudia; Luo, Beiping
    • Atmospheric Chemistry and Physics, Vol. 17, Issue 5
    • DOI: 10.5194/acp-17-3525-2017

    Nanomaterial–microbe cross-talk: physicochemical principles and (patho)biological consequences
    journal, January 2018

    • Westmeier, D.; Hahlbrock, A.; Reinhardt, C.
    • Chemical Society Reviews, Vol. 47, Issue 14
    • DOI: 10.1039/c6cs00691d

    Stabilization of AgI's polar surfaces by the aqueous environment, and its implications for ice formation
    journal, January 2019

    • Sayer, Thomas; Cox, Stephen J.
    • Physical Chemistry Chemical Physics, Vol. 21, Issue 27
    • DOI: 10.1039/c9cp02193k

    Refreeze experiments with water droplets containing different types of ice nuclei interpreted by classical nucleation theory
    journal, January 2017

    • Kaufmann, Lukas; Marcolli, Claudia; Luo, Beiping
    • Atmospheric Chemistry and Physics, Vol. 17, Issue 5
    • DOI: 10.5194/acp-17-3525-2017