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Saturn-Shaped Ice Burst Pattern and Fast Basal Binding of an Ice-Binding Protein from an Antarctic Bacterial Consortium

  • Aleksei Kaleda
    Aleksei Kaleda
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
    Department of Chemistry and Biotechnology, School of Science, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn, Estonia
  • Lotem Haleva
    Lotem Haleva
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
    More by Lotem Haleva
  • Guy Sarusi
    Guy Sarusi
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
    More by Guy Sarusi
  • Tova Pinsky
    Tova Pinsky
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
    More by Tova Pinsky
  • Marco Mangiagalli
    Marco Mangiagalli
    Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy
  • Maya Bar Dolev
    Maya Bar Dolev
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
  • Marina Lotti
    Marina Lotti
    Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy
    More by Marina Lotti
  • Marco Nardini
    Marco Nardini
    Department of Biosciences, University of Milano, Via Celoria 26, 20133 Milan, Italy
  • , and 
  • Ido Braslavsky*
    Ido Braslavsky
    Institute of Biochemistry, Food Science and Nutrition, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7610001, Israel
    *E-mail: [email protected]. Tel: +972-54-8820955.
Cite this: Langmuir 2019, 35, 23, 7337–7346
Publication Date (Web):September 10, 2018
https://doi.org/10.1021/acs.langmuir.8b01914
Copyright © 2018 American Chemical Society

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    Abstract

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    Ice-binding proteins (IBPs) bind to ice crystals and control their growth, enabling host organisms to adapt to subzero temperatures. By binding to ice, IBPs can affect the shape and recrystallization of ice crystals. The shapes of ice crystals produced by IBPs vary and are partially due to which ice planes the IBPs are bound to. Previously, we have described a bacterial IBP found in the metagenome of the symbionts of Euplotes focardii (EfcIBP). EfcIBP shows remarkable ice recrystallization inhibition activity. As recrystallization inhibition of IBPs and other materials are important to the cryopreservation of cells and tissues, we speculate that the EfcIBP can play a future role as an ice recrystallization inhibitor in cryopreservation applications. Here we show that EfcIBP results in a Saturn-shaped ice burst pattern, which may be due to the unique ice-plane affinity of the protein that we elucidated using the fluorescent-based ice-plane affinity analysis. EfcIBP binds to ice at a speed similar to that of other moderate IBPs (5 ± 2 mM–1 s–1); however, it is unique in that it binds to the basal and previously unobserved pyramidal near-basal planes, while other moderate IBPs typically bind to the prism and pyramidal planes and not basal or near-basal planes. These insights into EfcIBP allow a better understanding of the recrystallization inhibition for this unique protein.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.8b01914.

    • Figure S1. Ice crystal growth and burst in 10 μM EfcIBP (A–H) and in 25 μM GFP-EfcIBP (I–P). Letters indicate the sequence of frames (PDF)

    • Figure S2. Models of ice crystal shapes formed in EfcIBP solutions. (A) Hexagonal bifrustum, ice crystal shape formed by the T67Y mutant. (B) A simplified model of Saturn-shaped burst perpendicular to the c-axis. For simplicity, the example is given for the T67Y mutant (PDF)

    • Figure S3. Thermal hysteresis activity of EfcIBP compared to GFP-EfcIBP. Each point presents the average of three independent measurements, with 95% confidence intervals (PDF)

    • Figure S4. GFP-tagged EfcIBP accumulation on ice crystals. Colored rectangles show areas of fluorescence intensity measurements: red, basal plane (truncated sheet); yellow, pyramidal plane (crystal side); cyan, background (PDF)

    • Figure S5. EfcIBP mutation sites. Mutated residues on the B (yellow) and C (green) faces of the EfcIBP structure are shown as sticks and indicated by arrows and labels (PDF)

    • Figure S6. Ice crystal shapes and their growth pattern during cooling in solutions of EfcIBP mutants. The letters in parentheses indicate the protein face that was mutated. T67Y, T178Y, T223Y, and T209Y are 10 μM; S188Y is 3.3 μM; and T247Y is 50 μM. The circled dot indicates c-axis normal to the image plane (PDF)

    • Figure S7. GFP-EfcIBP mutants growth and burst after cooling below the TH freezing point, as seen between two coverslips. After the burst, the temperature is held constant. (A) GFP-T67Y mutant at 20 μM. (B) GFP-T223Y mutant at 17 μM. (C) GFP-T247Y mutant at 17 μM (PDF)

    • Movie S1. Ice crystal growth and burst in the wt EfcIBP 5 μM solution during cooling. The first 30 s are accelerated four times while the rest of the movie is in real time (AVI)

    • Movie S2. Ice crystals burst in 7.6 μM GFP-EfcIBP solution. A growing parallel ice sheet is blocked by a perpendicular ice sheet (tilted a-axis) (AVI)

    • Movie S3. Single ice crystal in 10 μM GFP-EfcIBP grown in a microfluidic chip with a height of 40 μm. Photos were taken with a time interval of 0.3 s. The edge of the microfluidic chip can be seen in the frame as curved lines around the ice crystal (AVI)

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    Cited By

    This article is cited by 12 publications.

    1. Yihang Gao, Haishan Qi, Lei Zhang. Advances in Antifreeze Molecules: From Design and Mechanisms to Applications. Industrial & Engineering Chemistry Research 2023, 62 (20) , 7839-7858. https://doi.org/10.1021/acs.iecr.3c00690
    2. Tero Kämäräinen, Kazunori Kadota, Jun Yee Tse, Hiromasa Uchiyama, Shinya Yamanaka, Yuichi Tozuka. Modulating the Pore Architecture of Ice-Templated Dextran Microparticles Using Molecular Weight and Concentration. Langmuir 2022, 38 (21) , 6741-6751. https://doi.org/10.1021/acs.langmuir.2c00721
    3. Tehilla Berger, Konrad Meister, Arthur L. DeVries, Robert Eves, Peter L. Davies, Ran Drori. Synergy between Antifreeze Proteins Is Driven by Complementary Ice-Binding. Journal of the American Chemical Society 2019, 141 (48) , 19144-19150. https://doi.org/10.1021/jacs.9b10905
    4. Bin Xue, Lishan Zhao, Xuehua Qin, Meng Qin, Jiancheng Lai, Wenmao Huang, Hai Lei, Jianjun Wang, Wei Wang, Ying Li, Yi Cao. Bioinspired Ice Growth Inhibitors Based on Self-Assembling Peptides. ACS Macro Letters 2019, 8 (10) , 1383-1390. https://doi.org/10.1021/acsmacrolett.9b00610
    5. Yuly Ximena Correa-González, Travis Clark Sena, Tao Wu. Chitin nanocrystals – A new material with ice-shaping and ice recrystallization inhibition activities. Food Hydrocolloids 2024, 150 , 109669. https://doi.org/10.1016/j.foodhyd.2023.109669
    6. Ran Drori, Corey A. Stevens. Divergent Mechanisms of Ice Growth Inhibition by Antifreeze Proteins. 2024, 169-181. https://doi.org/10.1007/978-1-0716-3503-2_12
    7. Tatsuya Arai, Akari Yamauchi, Yue Yang, Shiv Mohan Singh, Yuji C. Sasaki, Sakae Tsuda. Adsorption of ice-binding proteins onto whole ice crystal surfaces does not necessarily confer a high thermal hysteresis activity. Scientific Reports 2022, 12 (1) https://doi.org/10.1038/s41598-022-19803-3
    8. Irene Tagliaro, Alessio Cerpelloni, Vasileios-Martin Nikiforidis, Rohit Pillai, Carlo Antonini. On the Development of Icephobic Surfaces: Bridging Experiments and Simulations. 2022, 235-272. https://doi.org/10.1007/978-3-030-82992-6_8
    9. Santosh Kumar, Nurit Adiram-Filiba, Shula Blum, Javier Arturo Sanchez-Lopez, Oren Tzfadia, Ayelet Omid, Hanne Volpin, Yael Heifetz, Gil Goobes, Rivka Elbaum, . Siliplant1 protein precipitates silica in sorghum silica cells. Journal of Experimental Botany 2020, 71 (21) , 6830-6843. https://doi.org/10.1093/jxb/eraa258
    10. Maya Bar-Dolev, Koli Basu, Ido Braslavsky, Peter L. Davies. Structure–Function of IBPs and Their Interactions with Ice. 2020, 69-107. https://doi.org/10.1007/978-3-030-41948-6_4
    11. Surís-Valls, Voets. Peptidic Antifreeze Materials: Prospects and Challenges. International Journal of Molecular Sciences 2019, 20 (20) , 5149. https://doi.org/10.3390/ijms20205149
    12. Tyler D. R. Vance, Maddalena Bayer‐Giraldi, Peter L. Davies, Marco Mangiagalli. Ice‐binding proteins and the ‘domain of unknown function’ 3494 family. The FEBS Journal 2019, 286 (5) , 855-873. https://doi.org/10.1111/febs.14764

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