Ice-binding proteins that accumulate on different ice crystal planes produce distinct thermal hysteresis dynamics

Drori, Ran; Celik, Yeliz; Davies, Peter L.; Braslavsky, Ido

doi:10.1098/rsif.2014.0526

Cited by 80 publications

(199 citation statements)

References 49 publications

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“…Our experiments show that the NIBF can depress the formation of ice nuclei, and the NIBF of AFPs with a higher activity of TH exhibits higher activity in depressing ice nucleation. This finding may provide another explanation for various capabilities of different AFPs in depressing the freezing point, which was attributed to the binding of the AFPs to different crystal faces (20,43,44). All these findings show that both the IBF and the NIBF of AFPs are important, and they cooperatively work together rendering the AFPs having the capability of protecting living organisms at subzero conditions.…”

Section: Discussionmentioning

confidence: 76%

Janus effect of antifreeze proteins on ice nucleation

Liu

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

227

187

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The mechanism of ice nucleation at the molecular level remains largely unknown. Nature endows antifreeze proteins (AFPs) with the unique capability of controlling ice formation. However, the effect of AFPs on ice nucleation has been under debate. Here we report the observation of both depression and promotion effects of AFPs on ice nucleation via selectively binding the ice-binding face (IBF) and the non-ice-binding face (NIBF) of AFPs to solid substrates. Freezing temperature and delay time assays show that ice nucleation is depressed with the NIBF exposed to liquid water, whereas ice nucleation is facilitated with the IBF exposed to liquid water. The generality of this Janus effect is verified by investigating three representative AFPs. Molecular dynamics simulation analysis shows that the Janus effect can be established by the distinct structures of the hydration layer around IBF and NIBF. Our work greatly enhances the understanding of the mechanism of AFPs at the molecular level and brings insights to the fundamentals of heterogeneous ice nucleation.antifreeze proteins | ice nucleation | Janus effect | interfacial water | selective tethering A ntifreeze proteins (AFPs) protect a broad range of organisms inhabiting subzero environments. The function of AFPs lies in lowering the freezing point in a noncolligative manner (1, 2). It has been shown that AFPs can adsorb on the ice crystal surface with the ice-binding face (IBF, also termed ice-binding site or icebinding surface) (3, 4). The adsorbed AFPs lead to curvatures on the ice surface between adjacent AFPs, and ice growth is retarded due to the Kelvin effect, which is known as the adsorptioninhibition mechanism (5). However, whether the non-ice-binding face (NIBF) is involved in the function of AFPs and what effect the NIBF exerts are rarely studied (4, 6, 7). On the other hand, the effect of AFPs on ice nucleation (8) is still under intense debate (9-13), although ice nucleation, the formation of a stable nucleus with a critical size, is the control step for ice formation (8). Liu et al. (9) suggested that AFPs could inhibit heterogeneous ice nucleation of water, whereas research on ice nucleation of microdroplets of AFP solutions exhibited no obvious effect of AFPs in inhibiting ice nucleation (10). It was also reported that an AFP solution with high concentration facilitated ice nucleation (11). The contradiction also exists for the research of ice nucleation on solid surfaces immobilized with AFPs (12, 13). Therefore, it is highly desirable to elucidate the exact role of AFPs on ice nucleation and to correlate AFP structures at the molecular level with their function in tuning ice nucleation, which is essential for practical applications in food, pharmaceutical, and chemical industries (14,15).Herein, we investigate the effect of IBF and NIBF of AFPs on ice nucleation via binding AFPs to solid substrates in a way that either IBF or NIBF is exposed to liquid water. This binding method is readily extendable to other AFPs because of the clear distinction...

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Section: Discussionmentioning

confidence: 76%

Janus effect of antifreeze proteins on ice nucleation

Liu

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

227

187

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“…20,37,44 According to this hypothesis, the time required for irreversible adsorption of AFP type III molecules on the {101̅ y} planes is the shortest, whereas that on the {112̅ x} planes is the longest; the {112̅ x} planes need a longer time period to completely stop growing compared with the {101̅ y} plane ( Figure S9).…”

Section: Crystal Growth and Designmentioning

confidence: 93%

Pit Formation on the Basal Plane of Ice in Antifreeze Protein Type III Solution for Different Growth Mechanisms of Ice

Inada

Koyama

Funakoshi

2016

Crystal Growth & Design

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When a single crystal of ice that has the basal plane several tenths of mm 2 in area grows in a moderately active antifreeze protein (AFP) solution, numerous pits consisting of six pyramidal planes are formed on the basal plane. This pit formation suggests some interactions between the AFPs and the basal plane. In this study, we observed pit formation on the basal plane of ice growing in a 5 mg/mL fish AFP (type III) solution and examined three growth mechanisms (normal, spiral, and two-dimensional (2D) nucleation) of the basal plane by measuring the relationship between the growth rate and the degree of supercooling. We also measured the number density of pits in ice and found that the number density of pits for normal growth mode on molecularly rough surfaces was lower than that for spiral growth mode on relatively smooth surfaces, whereas pit formation was not observed during 2D nucleation growth mode. On the basis of these results, we proposed a model of pit formation during spiral growth mode. In this model, if only reversible adsorption of the AFP molecules on the smooth surfaces is considered to occur, then pit formation can be explained without assuming irreversible adsorption on the smooth surfaces.

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“…This apparent contradiction is due to the longer exposure time of nascent ice crystals to AFPs at a lower ice volume fraction in cryoscopy compared with sonocrystallization. The adsorption kinetics of AFPs also impacts TH activity and is known to depend on both AFP type and the ice plane of adsorption (36,37). Furthermore, no significant correlation is found between TH and IRI activities.…”

mentioning

confidence: 93%

Blocking rapid ice crystal growth through nonbasal plane adsorption of antifreeze proteins

Olijve

Meister

DeVries

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

146

167

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Antifreeze proteins (AFPs) are a unique class of proteins that bind to growing ice crystal surfaces and arrest further ice growth. AFPs have gained a large interest for their use in antifreeze formulations for water-based materials, such as foods, waterborne paints, and organ transplants. Instead of commonly used colligative antifreezes such as salts and alcohols, the advantage of using AFPs as an additive is that they do not alter the physicochemical properties of the water-based material. Here, we report the first comprehensive evaluation of thermal hysteresis (TH) and ice recrystallization inhibition (IRI) activity of all major classes of AFPs using cryoscopy, sonocrystallization, and recrystallization assays. The results show that TH activities determined by cryoscopy and sonocrystallization differ markedly, and that TH and IRI activities are not correlated. The absence of a distinct correlation in antifreeze activity points to a mechanistic difference in ice growth inhibition by the different classes of AFPs: blocking fast ice growth requires rapid nonbasal plane adsorption, whereas basal plane adsorption is only relevant at long annealing times and at small undercooling. These findings clearly demonstrate that biomimetic analogs of antifreeze (glyco)proteins should be tailored to the specific requirements of the targeted application.antifreeze protein | thermal hysteresis | ice recrystallization inhibition

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Ice-binding proteins that accumulate on different ice crystal planes produce distinct thermal hysteresis dynamics

Cited by 80 publications

References 49 publications

Janus effect of antifreeze proteins on ice nucleation

Janus effect of antifreeze proteins on ice nucleation

Pit Formation on the Basal Plane of Ice in Antifreeze Protein Type III Solution for Different Growth Mechanisms of Ice

Blocking rapid ice crystal growth through nonbasal plane adsorption of antifreeze proteins

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