Anchored clathrate waters bind antifreeze proteins to ice
Edited by Michael Levitt, Stanford University School of Medicine, Stanford, CA, and approved March 8, 2011 (received for review January 10, 2011)
Commentary
April 25, 2011
Abstract
The mechanism by which antifreeze proteins (AFPs) irreversibly bind to ice has not yet been resolved. The ice-binding site of an AFP is relatively hydrophobic, but also contains many potential hydrogen bond donors/acceptors. The extent to which hydrogen bonding and the hydrophobic effect contribute to ice binding has been debated for over 30 years. Here we have elucidated the ice-binding mechanism through solving the first crystal structure of an Antarctic bacterial AFP. This 34-kDa domain, the largest AFP structure determined to date, folds as a Ca2+-bound parallel beta-helix with an extensive array of ice-like surface waters that are anchored via hydrogen bonds directly to the polypeptide backbone and adjacent side chains. These bound waters make an excellent three-dimensional match to both the primary prism and basal planes of ice and in effect provide an extensive X-ray crystallographic picture of the AFP∶ice interaction. This unobstructed view, free from crystal-packing artefacts, shows the contributions of both the hydrophobic effect and hydrogen bonding during AFP adsorption to ice. We term this mode of binding the “anchored clathrate” mechanism of AFP action.
Data Availability
Data deposition: The atomic coordinates and structure factors have been deposited in the Research Collaboratory for Structural Bioinformatics Protein Data Bank, www.rcsb.org (RCSB PDB ID code 3P4G).
Acknowledgments.
We thank Jean Jakoncic and Vivian Stojanoff of the X6A beamline at Brookhaven National Laboratories for help with X-ray data acquisition and processing and Jack Gilbert for the initial discovery of M. primoryensisAFP. We also thank Dr. John Allingham for access to a Rigaku home X-ray source for initial diffraction experiments. This work was funded by the Canadian Institutes of Health Research. C.P.G. is the recipient of an Natural Sciences and Engineering Research Council of Canada three-year Postgraduate Scholarship (PGS D3). P.L.D. holds a Canada Research Chair in protein engineering.
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Freely available online through the PNAS open access option.
Data Availability
Data deposition: The atomic coordinates and structure factors have been deposited in the Research Collaboratory for Structural Bioinformatics Protein Data Bank, www.rcsb.org (RCSB PDB ID code 3P4G).
Submission history
Published online: April 11, 2011
Published in issue: May 3, 2011
Keywords
Acknowledgments
We thank Jean Jakoncic and Vivian Stojanoff of the X6A beamline at Brookhaven National Laboratories for help with X-ray data acquisition and processing and Jack Gilbert for the initial discovery of M. primoryensisAFP. We also thank Dr. John Allingham for access to a Rigaku home X-ray source for initial diffraction experiments. This work was funded by the Canadian Institutes of Health Research. C.P.G. is the recipient of an Natural Sciences and Engineering Research Council of Canada three-year Postgraduate Scholarship (PGS D3). P.L.D. holds a Canada Research Chair in protein engineering.
Notes
This article is a PNAS Direct Submission.
See Commentary on page 7281.
Authors
Competing Interests
The authors declare no conflict of interest.
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Anchored clathrate waters bind antifreeze proteins to ice, Proc. Natl. Acad. Sci. U.S.A.
108 (18) 7363-7367,
https://doi.org/10.1073/pnas.1100429108
(2011).
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