Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water

Steven J. Roeters; Thaddeus W. Golbek; Mikkel Bregnhøj; Taner Drace; Sarah Alamdari; Winfried Roseboom; Gertjan Kramer; Tina Šantl-Temkiv; Kai Finster; Jim Pfaendtner; Sander Woutersen; Thomas Boesen; Tobias Weidner

doi:10.1038/s41467-021-21349-3

Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water

Steven J. Roeters, Thaddeus W. Golbek, Mikkel Bregnhøj, Taner Drace, Sarah Alamdari, Winfried Roseboom, Gertjan Kramer, Tina Šantl-Temkiv, Kai Finster, Jim Pfaendtner, Sander Woutersen, Thomas Boesen, Tobias Weidner^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

55 Citationer (Scopus)

Abstract

Ice-nucleation active (INA) bacteria can promote the growth of ice more effectively than any other known material. Using specialized ice-nucleating proteins (INPs), they obtain nutrients from plants by inducing frost damage and, when airborne in the atmosphere, they drive ice nucleation within clouds, which may affect global precipitation patterns. Despite their evident environmental importance, the molecular mechanisms behind INP-induced freezing have remained largely elusive. We investigate the structural basis for the interactions between water and the ice-nucleating protein InaZ from the INA bacterium Pseudomonas syringae. Using vibrational sum-frequency generation (SFG) and two-dimensional infrared spectroscopy, we demonstrate that the ice-active repeats of InaZ adopt a β-helical structure in solution and at water surfaces. In this configuration, interaction between INPs and water molecules imposes structural ordering on the adjacent water network. The observed order of water increases as the interface is cooled to temperatures close to the melting point of water. Experimental SFG data combined with molecular-dynamics simulations and spectral calculations show that InaZ reorients at lower temperatures. This reorientation can enhance water interactions, and thereby the effectiveness of ice nucleation.

Originalsprog	Engelsk
Artikelnummer	1183
Tidsskrift	Nature Communications
Vol/bind	12
Nummer	1
Antal sider	9
ISSN	2041-1723
DOI	https://doi.org/10.1038/s41467-021-21349-3
Status	Udgivet - 1 dec. 2021

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10.1038/s41467-021-21349-3Licens: CC BY

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Aeromikrobiologi
Santl-Temkiv, T. (Projektleder), Finster, K. (Projektleder), Bilde, M. (PI), Weidner, T. (PI), Boesen, T. (PI), Melvad, C. (PI), Nielsen, M. B. (PI), Im, U. (PI), Sahyoun, M. (PI), Tesson, S. V. (PI), Dreyer, L. S. A. (PI), Rosati, B. (PI), Dwivedi, A. K. (PI), Jensen, L. Z. (PI) & Wieber, C. (PI)
Projekter: Projekt › Forskning

Citationsformater

Roeters, S. J., Golbek, T. W., Bregnhøj, M., Drace, T., Alamdari, S., Roseboom, W., Kramer, G., Šantl-Temkiv, T., Finster, K., Pfaendtner, J., Woutersen, S., Boesen, T., & Weidner, T. (2021). Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water. Nature Communications, 12(1), Artikel 1183. https://doi.org/10.1038/s41467-021-21349-3

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title = "Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water",

abstract = "Ice-nucleation active (INA) bacteria can promote the growth of ice more effectively than any other known material. Using specialized ice-nucleating proteins (INPs), they obtain nutrients from plants by inducing frost damage and, when airborne in the atmosphere, they drive ice nucleation within clouds, which may affect global precipitation patterns. Despite their evident environmental importance, the molecular mechanisms behind INP-induced freezing have remained largely elusive. We investigate the structural basis for the interactions between water and the ice-nucleating protein InaZ from the INA bacterium Pseudomonas syringae. Using vibrational sum-frequency generation (SFG) and two-dimensional infrared spectroscopy, we demonstrate that the ice-active repeats of InaZ adopt a β-helical structure in solution and at water surfaces. In this configuration, interaction between INPs and water molecules imposes structural ordering on the adjacent water network. The observed order of water increases as the interface is cooled to temperatures close to the melting point of water. Experimental SFG data combined with molecular-dynamics simulations and spectral calculations show that InaZ reorients at lower temperatures. This reorientation can enhance water interactions, and thereby the effectiveness of ice nucleation.",

author = "Roeters, {Steven J.} and Golbek, {Thaddeus W.} and Mikkel Bregnh{\o}j and Taner Drace and Sarah Alamdari and Winfried Roseboom and Gertjan Kramer and Tina {\v S}antl-Temkiv and Kai Finster and Jim Pfaendtner and Sander Woutersen and Thomas Boesen and Tobias Weidner",

note = "Funding Information: This article is part of a project that has received funding from the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 research and innovation program (Grant agreement no. 819039 F-BioIce). T.W., S.J.R. and T.{\v S}.T. thank the Villum Foundation for financial support (Experiment Grants 22956 and 23175). K.F. and T.{\v S}.T. also acknowledge the support by The Danish National Research Foundation (Grant agreement no.: DNRF106, to the Stellar Astrophysics Centre, Aarhus University). We thank Sean A. Fischer for support with the spectral calculations, and Rolf Mertig for help with the Mathematica code used to perform the spectral calculations. We thank Daniel Otzen for support with CD spectroscopy. S.A. would like to acknowledge funding from the National Science Foundation Graduate Research Fellowship Program under Grant no. DGE-1762114 to support this research. We thank S{\o}ren Jensen and Meilee Ling for help with the InaZ9R construct. The simulations were done on the Hyak supercomputer system funded in part by the STF at the University of Washington. We thank Andrey Kajava and Peter Davies for providing us with structure files for the InaZ models. Publisher Copyright: {\textcopyright} 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

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doi = "10.1038/s41467-021-21349-3",

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AU - Roeters, Steven J.

AU - Golbek, Thaddeus W.

AU - Bregnhøj, Mikkel

AU - Drace, Taner

AU - Alamdari, Sarah

AU - Roseboom, Winfried

AU - Kramer, Gertjan

AU - Šantl-Temkiv, Tina

AU - Finster, Kai

AU - Pfaendtner, Jim

AU - Woutersen, Sander

AU - Boesen, Thomas

AU - Weidner, Tobias

N1 - Funding Information: This article is part of a project that has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (Grant agreement no. 819039 F-BioIce). T.W., S.J.R. and T.Š.T. thank the Villum Foundation for financial support (Experiment Grants 22956 and 23175). K.F. and T.Š.T. also acknowledge the support by The Danish National Research Foundation (Grant agreement no.: DNRF106, to the Stellar Astrophysics Centre, Aarhus University). We thank Sean A. Fischer for support with the spectral calculations, and Rolf Mertig for help with the Mathematica code used to perform the spectral calculations. We thank Daniel Otzen for support with CD spectroscopy. S.A. would like to acknowledge funding from the National Science Foundation Graduate Research Fellowship Program under Grant no. DGE-1762114 to support this research. We thank Søren Jensen and Meilee Ling for help with the InaZ9R construct. The simulations were done on the Hyak supercomputer system funded in part by the STF at the University of Washington. We thank Andrey Kajava and Peter Davies for providing us with structure files for the InaZ models. Publisher Copyright: © 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Ice-nucleation active (INA) bacteria can promote the growth of ice more effectively than any other known material. Using specialized ice-nucleating proteins (INPs), they obtain nutrients from plants by inducing frost damage and, when airborne in the atmosphere, they drive ice nucleation within clouds, which may affect global precipitation patterns. Despite their evident environmental importance, the molecular mechanisms behind INP-induced freezing have remained largely elusive. We investigate the structural basis for the interactions between water and the ice-nucleating protein InaZ from the INA bacterium Pseudomonas syringae. Using vibrational sum-frequency generation (SFG) and two-dimensional infrared spectroscopy, we demonstrate that the ice-active repeats of InaZ adopt a β-helical structure in solution and at water surfaces. In this configuration, interaction between INPs and water molecules imposes structural ordering on the adjacent water network. The observed order of water increases as the interface is cooled to temperatures close to the melting point of water. Experimental SFG data combined with molecular-dynamics simulations and spectral calculations show that InaZ reorients at lower temperatures. This reorientation can enhance water interactions, and thereby the effectiveness of ice nucleation.

AB - Ice-nucleation active (INA) bacteria can promote the growth of ice more effectively than any other known material. Using specialized ice-nucleating proteins (INPs), they obtain nutrients from plants by inducing frost damage and, when airborne in the atmosphere, they drive ice nucleation within clouds, which may affect global precipitation patterns. Despite their evident environmental importance, the molecular mechanisms behind INP-induced freezing have remained largely elusive. We investigate the structural basis for the interactions between water and the ice-nucleating protein InaZ from the INA bacterium Pseudomonas syringae. Using vibrational sum-frequency generation (SFG) and two-dimensional infrared spectroscopy, we demonstrate that the ice-active repeats of InaZ adopt a β-helical structure in solution and at water surfaces. In this configuration, interaction between INPs and water molecules imposes structural ordering on the adjacent water network. The observed order of water increases as the interface is cooled to temperatures close to the melting point of water. Experimental SFG data combined with molecular-dynamics simulations and spectral calculations show that InaZ reorients at lower temperatures. This reorientation can enhance water interactions, and thereby the effectiveness of ice nucleation.

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DO - 10.1038/s41467-021-21349-3

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SN - 2041-1723

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JO - Nature Communications

JF - Nature Communications

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Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water

Abstract

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