The Dielectric Relaxation of Hydration Water in Native Collagen Fibrils

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The Dielectric Relaxation of Hydration Water in Native Collagen Fibrils Yael Kurzweil-Segev, Ivan Popov, Inna Solomonov, Irit Sagit, and Yuri Feldman J. Phys. Chem. B, Just Accepted Manuscript • Publication Date (Web): 09 May 2017 Downloaded from http://pubs.acs.org on May 16, 2017

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The Journal of Physical Chemistry

The Dielectric Relaxation of Hydration Water in Native Collagen Fibrils Y. Kurzweil-Segev1, Ivan Popov1,2, Inna Solomonov3, Irit Sagit3 and Yuri Feldman1* 1

The Hebrew University of Jerusalem, Department of Applied Physics, Edmond J. Safra Campus, Givat Ram, Jerusalem, 91904, Israel 2 Institute of Physics, Kazan (Volga Region) Federal University, 420008, Kremlevskaya str.18, Kazan, Tatarstan, Russia 3 Weitzman Institute of Science, Department of Biological Regulation, Rehovot, 761001, Israel

Abstract The dielectric relaxation of hydrated collagen powders was studied over a wide temperature and frequency range. We revealed two mechanisms of dielectric relaxation in hydration water that are driven by the migration of ionic and orientation defects. At high water fractions in powders (h>0.2), the hydration shell around the collagen triple helixes presents a spatial H-bonded network consisting of structural water bridges and cleft water channels. These two water phases provide the long-range paths for proton-hopping and orientation defect migration. At low water fractions (h0.3 an additional process appears between the HW and the “middle” process due to ice formation from (see Fig. 1a) excess water 36, 37

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(b)

0

τmax

T=138K-162K, ∆T=6K

10

h=0.26

Dielectric losses, Im[ε(f)]

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10

-1

10

-2

-1

1

10

10

10

3

5

10

Frequency, f [Hz]

Figure 1 a) Typical experimental data landscape for the imaginary part of the complex dielectric permittivity of hydrated collagen powder for h=0.16, 0.26, 0.33. The surfaces are shifted relative to each other for clarity only. The process related to the hydration water is depicted by a rectangle. b) Typical cross-sections of the hydration water process at h=0.26. Along with the main loss peak, the pronounced excess wing is observed at high frequencies. The red lines are the results of the fitting procedure. The solid blue line defines the contribution of the term described by Eq. (1), and the dotted line defines the Jonsher correction (see text).

Typical isothermal cross sections of the HW relaxation process are depicted in Figure 1b (where h=0.26). Note that this process is asymmetrical with a weakly expressed excess wing at high frequencies. However, at lower hydration levels (Sample 1, h=0.16) the HW process exhibits a symmetrical losses peak. For all samples, the peak frequencies ν max of the HW and ice processes (at h=0.3) follow an Arrhenius dependence, τmax = (2πν max )−1 = τ0 exp( Ea / RT ) , over the entire temperature and hydration ranges. Our data for τmax of the HW and ice processes, as well as data obtained in the same way in works

36, 37

are presented in Figure 2a, where we observed quite

good agreement between these results.

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(a)

280 260 240 4

10

220

200

Temperature, T [K] 180 160

140

Johari et al, ice Ih

Gainaru et. al.

τorient≈τmax h=0.33

2

10

τionic

h=0.33

τice

h=0.33

ice processes

HW processes

τorient≈τmax h=0.26 τionic

h=0.26

τorient≈τmax h=0.16 τionic

0

τ [sec]

10

Sample 5: DT, h=0.28

τorient≈τmax Sample 5: DT, h=0.28

-2

10

-4

10

-6

10

4

5

6

7

8

1000/T [1/K]

Temperature, T [K]

(b) 280 260

240 220

200

180

160

140 Johari et al, ice Ih

10

2

Gainaru et. al. h=0.7 (ice process) h=0.5 (ice process) h=0.4 (ice process)

10

10

Gainaru et. al. h=0.3 (HW process)

1

∆ε

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h=0.2 (HW process)

h=0.33 (HW process) h=0.33 (ice process) 0

h=0.26 (HW process) Sample 5: DT, h=0.28 (HW process) h=0.16 (HW process)

10

-1

4

5

6

7

8

1000/T [1/K]

Figure 2a) The Arrhenius plot of the relaxation time for hydrated collagen powders. The gray diamonds are the data of the bulk ice 49. The dashed lines represent the previous results for ice and HW processes obtained in work 36. The blue triangles represent the relaxation time of the ice process observed in our measurements at h=0.33. The filled blue, red, green and orange squares are associated with the HW process of different samples and depict the relaxation time τorient , while open blue, red green and orange circles indicate the τionic obtained from Eq.(1) (see text below). Error bars for open blue circles appears due to influence of ice process on the fitting procedure; for other parameters fitting error within the symbol. b) The dielectric strength of the HW and ice processes. The gray diamonds are the data of the


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bulk 49. The grey stars, squares and triangles depict the ice process, whereas the black open squares and circles represent the HW process in hydrated collagen powders taken from 36. The blue triangles correspond to the ice process in our measurements at h=0.33. The blue, red, green and orange squares depict ∆ε(T ) for HW process in our measurements at h=0.33, 0.26, 0.16 and Sample 5 (partial DT) at h=0.28, respectively.

The observed asymmetry of the HW peak and excess wing in our results requires special attention in view of the influence of the protein structure on its hydration shell dynamics since this HW process doesn’t appear in globular proteins collagen

36, 37

50

. In recent dielectric studies of hydrated

these peculiarities are explained by the asymmetric distribution of relaxation times

and their barriers. In the following sections, we propose another consideration of this problem.

Mechanisms of the dielectric relaxation of hydration water Based on the NMR relaxation measurements of hydrated proteins

33, 35, 37-39

it has been

proposed that the reorientation mechanism of water molecules is that of large-angle jumps in different directions. In other words, the water rotation dynamics in hydrated collagen is better described by a wait-and-switch mode, rather than continuous diffusion. It resembles the similar relaxation mechanism in bulk ice

35, 51, 52

Bjerrum’s L-D orientation defects

53-55

, where relaxation is driven by the migration of the

and ionic defects OH-/ H3O+ via proton hopping

52, 56

.

Thus, the mechanisms of the dipole reorientation of water molecules in ice can be applied and tested in the description of the dielectric relaxation of water in hydrated proteins. Recently, we improved the model of an ice dielectric relaxation where both types of defect are considered 51. It was shown that if the mean square displacement of the defect obeys the following law: r 2 (t ) ~ t α , (here α is attributed to the degree of diffusion anomaly), we can write

ε* (ω) = ε∞ +

∆ε 1 + (iωτorient ) −αorient + (iωτionic )−αionic 

−1

,

(1)

where parameters τ orient and τionic define the relaxation times of the orientation and ionic defects respectively; ∆ε defines the dielectric strength; ε∞ is the high frequency limit of complex dielectric permittivity. Applying this equation for data processing, we obtained a good fit of the dielectric spectra (See Figure 1b). We can see that Eq. (1) allows us to describe the dielectric spectra over the entire frequency range with good accuracy. The temperature dependences of the 7 ACS Paragon Plus Environment


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fitting parameters ∆ε and relaxation times τorient , τionic for Samples S1, S2, S3 and S5 are β presented in Figure 2a and 2b. Note that in the fitting procedure, Jonsher’s correction A / (iω)

was used in order to take the combined residual influence of the low frequency processes into account. Furthermore, for Sample S3 (hydration level h=0.33) we included an additional ColeCole process due to the ice structure formation. Figure 2 shows that the temperature dependences of the fitting parameters τorient and τionic of the HW process demonstrate a tendency similar to that of the relaxation time behavior of the bulk ice τice at the low and middle temperature intervals. Furthermore, at the hydration levels h=0.26 and 0.33, when τionic (T ) meets τorient (T ) , these relaxation times proceed together towards the low temperature interval. Whereas for Samples S5 (h=0.28) and S1 (h=0.16) the relaxation time τionic (T ) ≈ τorient (T ) , and τionic (T ) = τorient (T ) , for the whole temperature range, respectively. It is worth noting that the time, which is associated with the maximum of the loss peak of the HW process τmax (see Figure 2b), is approximately equal to τorient . The energy of activation for the times τorient and τionic are presented in Table 2.

Table 2. The activation energies for the orientation, τorient , and ionic, τionic , mechanisms of relaxation of the hydration water in collagen powder. S1 (h=0.16) S2 (h=0.26) S3 (h=0.33) S5 (DT and hydrating by IE, h=0.28) Ea≈51 kJ/mol Ea≈58 kJ/mol Ea≈58 kJ/mol Ea≈51 kJ/mol τ orient

τionic

-

Ea≈16 kJ/mol

Ea≈16 kJ/mol

Ea≈46 kJ/mol

The dielectric strength of the HW process, with the exception of Sample S5, demonstrates growth typical to the hydration level (See Fig. 2b). The case of S5 is exceptional most probably because DT was applied to this sample. Furthermore, the temperature dependences of the dielectric strength of hydration water and ice processes display different slopes. It is well-known 57

that a positive slope (in the plane ∆ε vs 1/ T ) corresponds to a dipole disordered system,

whereas a negative slope corresponds to a dipole ordered one. Figure 2b shows that the hydration water of collagen exhibits a more ordered dipole structure in comparison with ice.


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Thus, two dielectric relaxation mechanisms exist in the hydration water in collagen. They are characterized by the two relaxation times τorient and τionic , the temperature dependences of which are similar to that of the relaxation time of the bulk ice (as can be observed in Fig. 2a). Therefore, to obtain more information regarding these relaxation mechanisms we must recollect and discuss what we know about dielectric relaxation in ice. To simplify the discussion, we reproduce a schematic representation of Figure 2, keeping only those relaxation times corresponding to the bulk Ih ice and HW processes (See Fig 3). The relaxation mechanisms in bulk ice at the high and middle temperature range were examined in detail

51, 58

. There it was concluded that the origin of the sharp temperature crossover at

Tc≈230±3K is a transformation of the relaxation mechanism driven by the diffusion of Bjerrum L-D

53

orientation defects to one where the diffusion of intrinsic ionic OH-/H3O+ defects is

dominant. However, the nature of the second, smoother crossover at low temperatures was not quite understood. The close energy activation values of the high and low temperature ranges (as can be seen from the slopes of the ice curve in Fig. 3) suggests that the second crossover is a transition back to the mechanism of the orientation defects or something similar. One of the explanation may be attributed to the suppressing of the ionic defects diffusion by the L-D defects59. In fact, the orientation Bjerrum defects may create a blockage for proton hopping from one water molecule to another

58, 59

. At high temperatures, the retention time of ionic defect in

traps is not so long due to its fast diffusion. However, at low temperatures due to the slowing down of the orientation L-D defects the ionic defects may be trapped for the long time-period. It leads to increase of the relaxation time and originates the low temperature crossover. Another explanation may be related to the fact that at low temperatures, ice loses its continuous integrity due to the appearance of self-interstitial defects

60-62

. The diffusion of the self-interstitials in ice

leads to the growth of dislocation loops, which implies a breach in the integrity of the bulk ice structure and the appearance of interfacial regions in the interior. On the other hand, these microscopic cracks in the ice prevent the long-range diffusion of ionic defects

63-69

, suppressing

their role in the dielectric relaxation mechanism in ice as well. Drawing an analogy between the relaxation times of ice and hydration water in collagen, we can present the latter as an extremely porous ice-like layer around the collagen triple helixes. Therefore, as well as in works

35, 70

, we introduced two mechanisms of relaxation in the

hydration water in collagen in Eq.(1): orientation and ionic defects migration. At high hydration 9 ACS Paragon Plus Environment


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levels (h=0.26 and 0.33), we suggest that this ice-like structure consists of structural water bridges connected by cleft water chains. Together, these two water compartments create the expanded H-bond network around the collagen triple helix, which provide the paths for longrange proton and orientation defect migration. Therefore, at hydration levels of more than 0.2 we observe two different relaxation time temperature behaviors. However, the dominant relaxation mechanism is orientation defect migration, since the maximum of the loss peak is defined by

τmax ≈ τorient (see Fig. 2a). Furthermore, the relaxation time corresponding to proton hopping (ionic defect), is faster here than in ice. This is probably due to the fact that in the ice, the concentration of protons is defined only by auto-ionization processes, whereas in the hydration water the protons from the protein surface may also participate in the relaxation process 70. Thus, the effective concentration of protons in hydration water is higher than that in ice, which causes the faster relaxation time. The bending in relaxation time of the ionic defects τionic similar to bulk ice is related to the suppressing of the ionic defects diffusion by the L-D defects, as described above. Due to this reason, when the branches τionic (T ) and τorient (T ) meet, τionic (T ) starts to follow τorient (T ) . In other words, the global migration of ionic defects cannot be faster than the diffusion of the orientation defects. Similarly, we obtain τionic (T ) ≈ τorient (T ) at the hydration level h=0.16 over the entire temperature range. In this case, the structural water phase is complete, but the cleft water phase is missing. The absence of the cleft water chains prevents the long-range migration of proton hopping and orientation defects. The relaxation occurs only in confined spaces, where contributions from the different mechanisms are comparable.


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Figure 3. Schematic representation of the relaxation times of the bulk ice (grey line) and HW process in hydrated collagen powders (colored lines).

The effect of Dehydrothermal Treatment (DT) on hydration water structure. One of the most unusual and surprising results we obtained is related to Sample S5. Its water fraction is comparable to that of Sample S2, however its relaxation times behave similarly to those of Sample S1. To reveal the influence of the DT on the collagen structure, we performed the TEM measurements before (Sample S4) and after (Sample S6) DT (as detailed in the materials methods section). TEM images (see Fig. 4a, b) show that upon heating, the fundamental periodicity (D-periodic stagger) of the collagen changed from 68±2nm to 62±2nm. This constriction is the result of tilting chains in the gap region that occurs during the DT (Fig.4c) 40. The tilting is related to the loss of water, including the loss of cleft water and structural water bridges from the collagen fibrils. The subsequent hydration of the sample for the BDS measurements does not seem to recover these two types of water compartments (it is likely there was not enough time for water to penetrate and rebuild the structural bridges and cleft water chains). 11 ACS Paragon Plus Environment


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Figure 4 a) TEM image of Sample S4; b) TEM image of Sample S6, after DT. The fundamental periodicity decreases from 68nm to 62 nm; c) The schematic representation of D-periodic stagger in collagen fibrils before and after DT 40. Each line represents a collagen triple helix 25.

Indeed, the relaxation times of the ionic and orientation defects in this sample are close in value, i.e. τionic (T ) ≈ τorient (T ) . Comparing this with the result of Sample S1, we may infer that the water content in Sample S5 is concentrated locally. Thus, although the water fraction in Sample S5 is high (h=0.28), the damage to the collagen matrix after DT leads to inability of the water to create a continuous spatial extended H-bond network. In turn, this prevents long-range defect migration.

Conclusion In this work, we have examined the relaxation mechanisms of hydration water in fibrillar collagen. Using BDS, we studied three samples with different hydration levels and one hydrated sample after DT. In the samples with high hydration levels (h >0.2) we revealed two mechanisms of dielectric relaxation of hydrated water: Ionic and orientation defect migration. Defect movement occurs through the spatial continuous H-bond water network around the collagen 12 ACS Paragon Plus Environment

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triple-helixes, which consists of structural water bridges and cleft water. In these cases, the mechanism driven by orientation defects is dominant. At low hydration levels, the water fraction is not sufficient to create the water cleft channels, and relaxation occurs in the local water compartments where the contributions of ionic and orientation defects are comparable. A similar situation occurs in the sample after DT. However, in this case, the tilting of the collagen chains prevents the creation of a continuous spatial hydration shell. It seems that even at hydration levels higher than h>0.2, water concentrates in local individual clusters.

Acknowledgments IP acknowledges the partial support by Russian Government Program of Competitive Growth of Kazan Federal University.



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(37) Lusceac, S. A.; Rosenstihl, M.; Vogel, M.; Gainaru, C.; Fillmer, A.; Bohmer, R. NMR and Dielectric Studies of Hydrated Collagen and Elastin: Evidence for a Delocalized Secondary Relaxation. J Non-Cryst Solids 2011, 357, 655-663. (38) Lusceac, S. A.; Vogel, M. R.; Herbers, C. R. H-2 and C-13 NMR Studies on the Temperature-Dependent Water and Protein Dynamics in Hydrated Elastin, Myoglobin and Collagen. Bba-Proteins Proteom 2010, 1804, 41-48. (39) Vogel, M. Origins of Apparent Fragile-to-Strong Transitions of Protein Hydration Waters. Phys Rev Lett 2008, 101. (40) Wess, T. J.; Orgel, J. P. Changes in Collagen Structure: Drying, Dehydrothermal Treatment and Relation to Long Term Deterioration. Thermochim Acta 2000, 365, 119-128. (41) Jansson, H.; Swenson, J. The Protein Glass Transition as Measured by Dielectric Spectroscopy and Differential Scanning Calorimetry. Bba-Proteins Proteom 2010, 1804, 20-26. (42) Khodadadi, S.; Pawlus, S.; Roh, J. H.; Sakai, V. G.; Mamontov, E.; Sokolov, A. P. The Origin of the Dynamic Transition in Proteins. J Chem Phys 2008, 128. (43) Khodadadi, S.; Pawlus, S.; Sokolov, A. P. Influence of Hydration on Protein Dynamics: Combining Dielectric and Neutron Scattering Spectroscopy Data. J Phys Chem B 2008, 112, 14273-14280. (44) Nakanishi, M.; Sokolov, A. P. Protein Dynamics in a Broad Frequency Range: Dielectric Spectroscopy Studies. J Non-Cryst Solids 2015, 407, 478-485. (45) Panagopoulou, A.; Kyritsis, A.; Aravantinou, A. M.; Nanopoulos, D.; Serra, R. S. I.; Ribelles, J. L. G.; Shinyashiki, N.; Pissis, P. Glass Transition and Dynamics in Lysozyme-Water Mixtures Over Wide Ranges of Composition. Food Biophys 2011, 6, 199-209. (46) Panagopoulou, A.; Kyritsis, A.; Shinyashiki, N.; Pissis, P. Protein and Water Dynamics in Bovine Serum Albumin-Water Mixtures over Wide Ranges of Composition. J Phys Chem B 2012, 116, 4593-4602. (47) Khodadadi, S.; Curtis, J. E.; Sokolov, A. P. Nanosecond Relaxation Dynamics of Hydrated Proteins: Water versus Protein Contributions. J Phys Chem B 2011, 115, 6222-6226. (48) Shinyashiki, N.; Yamamoto, W.; Yokoyama, A.; Yoshinari, T.; Yagihara, S.; Kita, R.; Ngai, K. L.; Capaccioli, S. Glass Transitions in Aqueous Solutions of Protein (Bovine Serum Albumin). J Phys Chem B 2009, 113, 14448-14456. (49) Johari, G. P.; Whalley, E. The Dielectric-Properties of Ice Ih in the Range 272-133-K. J Chem Phys 1981, 75, 1333-1340. (50) Kurzweil-Segev, Y.; Greenbaum, A.; Popov, I.; Golodnitsky, D.; Feldman, Y. The Role of the Confined Water in the Dynamic Crossover of Hydrated Lysozyme Powders. Phys Chem Chem Phys 2016, 18, 10992-10999. (51) Popov, I.; Puzenko, A.; Khamzin, A.; Feldman, Y. The Dynamic Crossover in Dielectric Relaxation Behavior of Ice I-h. Phys Chem Chem Phys 2015, 17, 1489-1497. (52) von Hippel, A. The Dielectric-Relaxation Spectra of Water, Ice, and Aqueous-Solutions, and Their Interpretation .3. Proton Organization and Proton-Transfer in Ice. Ieee T Electr Insul 1988, 23, 825-840. (53) Bjerrum, N. Structure and Properties of Ice. Science 1952, 115, 385-390. (54) Sciortino, F.; Geiger, A.; Stanley, H. E. Effect of Defects on Molecular Mobility in Liquid Water. Nature 1991, 354, 218-221. (55) Sciortino, F.; Geiger, A.; Stanley, H. E. Network Defects and Molecular Mobility in Liquid Water. J Chem Phys 1992, 96, 3857-3865. (56) Agmon, N. The Grotthuss Mechanism. Chem Phys Lett 1995, 244, 456-462. 16 ACS Paragon Plus Environment

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TOC Figure


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Figure 1a 172x171mm (300 x 300 DPI)

ACS Paragon Plus Environment


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Figure 1b 208x159mm (300 x 300 DPI)


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Figure 2a 208x159mm (300 x 300 DPI)



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Figure 2b 208x159mm (300 x 300 DPI)


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Figure 3 169x132mm (300 x 300 DPI)



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Figure 4a and 4b 46x77mm (300 x 300 DPI)


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Figure 4c 92x95mm (300 x 300 DPI)



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TOC graphs 84x65mm (300 x 300 DPI)


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Table 1. The hydrated collagen samples measured by BDS and TEM S1 Hydrating by IE

S2 Hydrating by IE

S3 Hydrating by IE

S4 Hydrating by IE

S5 DT and hydrating by IE

S6 DT and hydrating by IE

Water fraction

h=0.16

h=0.26

h=0.33

h=0.28

Fully solvated

Measurement technique

BDS

BDS

BDS

h=0.16 and then fully solvated TEM

BDS

TEM

Preparation method

Table 2. The activation energies for the orientation, orient , and ionic, ionic , mechanisms of relaxation of the hydration water in collagen powder. S1 (h=0.16) S2 (h=0.26) S3 (h=0.33) S5 (DT and hydrating by IE, h=0.28) E ≈51 kJ/mol E ≈58 kJ/mol E ≈58 kJ/mol E ≈51 kJ/mol a a a a  orient

ionic

-

Ea≈16 kJ/mol

Ea≈16 kJ/mol


Ea≈46 kJ/mol

The Dielectric Relaxation of Hydration Water in Native Collagen Fibrils

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