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Temperature evolution of hydration shells in solid DNA didecyldimethylammonium chloride complex studied by 1H NMR spectroscopy
European Polymer Journal 66 (2015) 301–306
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Temperature evolution of hydration shells in solid DNA didecyldimethylammonium chloride complex studied by 1H NMR spectroscopy Jacek Nizioł a,⇑, Piotr Nowak b, Jan Kobierski b, Hubert Haran´czyk b a b
AGH University of Science and Technology, Faculty of Physics and Applied Computer Science, al. Mickiewicza 30, 30-059 Kraków, Poland Jagiellonian University, Institute of Physics, ul. Łojasiewicza 11, 30-348 Kraków, Poland
a r t i c l e
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Article history: Received 18 January 2015 Received in revised form 18 February 2015 Accepted 22 February 2015 Available online 26 February 2015 Keywords: DNA–lipid complex Hydration 1 H NMR spectroscopy Biomaterials Bound water
a b s t r a c t In the case of DNA and its derivatives hydration effect are of paramount importance for many characteristics. Despite years of extensive research this phenomenon is not completely understood yet. A model DNA–lipid complex with didecyldimethylammonium chloride was subjected to gaseous phase hydration procedure. Using 1H NMR spectroscopy a qualitative change in hydration pattern was identified when the material was conditioned in atmosphere of 10.1% of relative humidity. At the threshold hydration level on the top of the first hydration shell appear water molecules that may be attributed to the second hydration shell. This value is lower, that cited in the bibliography as the saturation point of the first hydration level. Ó 2015 Elsevier Ltd. All rights reserved.
Deoxyribonucleic acid (DNA) is a vehicle carrying genetic information, thus since its discovery, it is most frequently discussed as mainly responsible for the mystery of life. However, from the chemical point of view, DNA is only a biopolymer with very particular and rare properties, resulting from its ‘‘intelligent’’ structure. DNA is a polynucleotide chain consisting of alternating phosphate units monosaccharide (deoxyribose) with bound one of four possible heterocyclic bases. Stable hydrogen bonds occur exclusively between base pairs adenine–thymine and guanine–cytosine. Thus, two single DNA strands of opposite base sequences can bind each to other forming a double stranded helix [26]. Strong affinity to water is inherent property of biomaterials, and in particular of DNA. The native DNA contains a significant amount of bound water. Water is not equally distributed within the DNA helix. There exist a continuum
⇑ Corresponding author. E-mail address: [email protected] (J. Nizioł). http://dx.doi.org/10.1016/j.eurpolymj.2015.02.037 0014-3057/Ó 2015 Elsevier Ltd. All rights reserved.
of states represented by water molecules hydrating chemically compatible sites on the helix surface. It has been widely accepted for a long time [35] an intuitive, simplified description of DNA hydration in terms of discrete hydration shells, the primary and the secondary one. Infrared spectroscopy provided evidence that completely filled primary shell consists of about 20 water molecules per nucleotide (wpn). It is achieved in equilibrium with the surrounding atmosphere at least 80% of relative humidity (RH). Water molecules in the primary shell differ in properties from bulk water. These molecules do not form ice crystallites even at temperatures well below 0 °C [8,25]. They are tightly bound and are essential to ensure stability of DNA microstructure [5]. Thus, it is virtually impossible to entirely remove water from DNA [43]. Water in the second hydration shell can be hardly distinguish from the bulk water [46]. The most important secondary conformations of DNA molecule, are referenced to as right-handed double-helical forms of the type A, B, C, D, and the left handed double-helical Z form. At room temperature, and at >90% RH solid
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DNA adopts B conformation. Upon dehydration form B undergoes some conformational transitions (to e.g. A or C form) depending on bases sequence, bound counterions, and other environmental conditions [46,45]. Extreme dehydration introduces a disordered state of DNA, which is characterized by a collapse of base stacking [49,37,20]. The rehydration process reverts these changes [7,49]. Dehydration is accompanied by a two-step decrease in conductivity of DNA samples [44]. Theoretical simulations indicate percolation within hydrogen-bonded water molecule network on DNA surface as the origin of critical phenomena related to hydration [3]. Organic electronics and photonics need materials in form of solid thin films of micron or of submicron thickness. Such films prepared from DNA derivatives combine unique optical and electronic properties [10]. Polymeric materials are typically processed into thin films through a variety of solution based techniques. In its natural environment, in every living cell, DNA exists in aqueous medium. Water evaporates slowly and it has high surface tension. This makes water difficult as the solvent for routine processing of polymeric materials. The natural water-soluble DNA-Na + salt can be treated with an amphiphilic cationic surfactant, to obtain complex that is insoluble in water but soluble in organic solvents, as alcohols [32]. It was shown that the cationic surfactants cooperatively bind to negatively charged DNA molecules in dilute solutions [23]. Stiffness differs the DNA molecule from majority of synthetic polymers. DNA double helix is a rigid cylinder with a diameter of about 2 nm and with persistence length of more than 30 nm [26]. Therefore, it cannot be wrapped easily around the surfactant micelles as in the case of synthetic polymers. DNA–surfactant complexes condensate to a compact, dense form [24] which may adopt lamellar or inverted hexagonal structure [18,2]. Overall properties of DNA and DNA–surfactant complexes in solid form very much differ from the long-time studied DNA dissolved in water [29]. Thin films from DNA–lipid complexes can be prepared either on substrates or as free standings. The choice of surfactant molecule determines mechanical properties of the free standing films, that can be brittle [22] or enough elastic to be stretch orientated [31]. At present, derivatives of DNA and different surfactants are considered as interesting material for a variety of applications. There are many reports on fully functional devices like organic light emitting diodes (OLED) [13,40,11], organic field effect transistors (OFET) [39,33], fuel cells [21,34], or lasers [48]. Extensive research concerning DNA based materials is also carried out in the field of nonlinear optics [27,36,41,42]. Lipid-based DNA formulations are also extensively studied in biochemistry and medicine for applications in modern gene therapy [47] and for pharmaceuticals administration [4]. However, there is still running debate how far DNA condensed with a cationic surfactant retains affinity to water, however significantly weaker. For example, in the case of the most extensively investigated DNA complex with hexadecyltrimetyl ammonium chloride (CTMA), at 80% RH materials’ moisture uptake attains about half of the value for native DNA [19,16]. Nevertheless, little is known about the behavior of the
complexes at low hydration form. Temporally stable properties of devices including a DNA–surfactant complex cannot be achieved without this knowledge. In our previous papers [15,30] we presented a hydration kinetics of a model complex of DNA and didecyldimethyl-ammonium chloride (DDCA), studied by 1H NMR spectroscopy. In the NMR signal we identified three component distinctly different in molecular mobility, manifesting as different values of relaxation times T⁄2 (spin–spin), and T1 (spin–lattice). These components were assigned to the solid state fraction and water from two hydration shells. Surprisingly, signal from the mobile water fraction appeared already at relatively low hydrations. The mass uptake at the threshold corresponded to c.a. 4–5 water molecules per nucleotide. In the current work we studied samples at increasing hydrations surrounding this threshold value. The research was enlarged by including thermal evolution of hydration depended variation of spin–spin relaxation. We believe that this approach yields a more precise insight into water dynamics at the critical hydration level. 1. Materials DNA extracted from salmon milt and roe was purchased from CIST (Chitose Institute of Science and Technology, Japan). DNA complex was prepared using double didecyldimethylammonium chloride (DDCA), an amphiphilic lipid consisting of cationic quaternary ammonia ‘‘head’’ and two alkyl ‘‘tails’’. The synthesis was based on simple ion-exchange reaction and has already been described in details elsewhere [28]. The obtained material was dried in ambient conditions and grinded in agate mortar into a fine powder. 2. Experimental DNA and its derivatives have natural affinity for water, to the extent that often water is considered as an inseparable constituent of DNA [35]. Therefore, the ‘‘dry mass’’ strongly depends on experimental procedure used for determination. To our best knowledge, any method is widely accepted as a standard procedure. It is known that heat [17] and vacuum [1] may irreversibly modify DNA microstructure. Disintegration of DNA complexes to low molecular mass compounds occurs at temperatures as high as above 200 °C [28]. From the other side, the exact kinetics and mechanisms involved in dehydration of DNA complexes are still unclear. Thus, excessive heating causes risk for the sample microstructure which can be irreversibly modified, even though the chemical composition is still unchanged. Therefore we suggest our standard DNA dehydration mode as follows. At first, the sample is stored in a desiccator over silica-gel. As soon as the mass of the sample reached a constant value, the sample is transferred into a vacuum dryer and stored there at 70° for 12 h. In result, the ‘‘silica-gel dry’’ DNA-DDCA sample loses c.a. 7.5% of its mass. At 70 °C DNA complexes are thermally stable, as proved by IR spectroscopy and by X-ray diffractometry [28,38]. In many 1H NMR experiments involving ‘‘dry’’
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DNA complexes, dried according to different protocols, we detected only one broad Gaussian line. Such a line is usually assigned to immobilized protons of the solid phase. Therefore, we prefer to define hydration level in terms of RH of the incubation atmosphere, where initially ‘‘dry’’ sample is stored as long as constant mass is reached. This approach seems more reasonable than at first claim a value to be the ‘‘true’’ dry mass and next, after hydration procedure, calculate water uptake. Controlled hydration of the samples was achieved by incubation in desiccators, over saturated aqueous salt solutions. The chosen series of solution provided relative humidity (RH) from 5% to 44%. A preliminary research suggested a qualitative breakthrough in DNA-DDCA hydration pattern within these range. RH values are used in the further text as references for samples. 1 H NMR spectra were collected using Bruker Avance III spectrometer with p/2 pulse series. The spectrometer was equipped with a thermo-controlled sample compartment and superconducting magnet providing magnetic field B0 = 7 T. The resonance frequency for protons was 300.13 MHz, the p/2 pulse duration 2.2 ls, the repetition rate 2 s and the power 400 W. To eliminate error due to statistically occurring material differences, all experiments were performed using the same DNA-DDCA sample. After each experimental series, the sample was dehydrated then hydrated to a next, higher level. NMR spectra were collected at temperatures decreased from the ambient to 55 °C, then raised, to avoid premature denaturation, to not more than 70 °C. Spectra recorded at cryogenic temperatures were identical regardless the direction of the temperature course.
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Independently, it was verified that the recorded signal pattern did not vary below 55 °C.
3. Results and discussions A distinct visual difference of the recorded NMR spectra is observed as hydration level increases. Exemplary stack plots of NMR signals are presented in Fig. 1. For the sake of space economy, in this figure are shown exclusively signals for extreme hydration levels (5% and 44%) and for two hydration levels (10.1% and 15.6%), where a threshold transition occurs. In Fig. 1(b) for 10.1% hydration level, spectra are featureless across entire temperature span, while in the next Fig. 1(c) for 15.6% hydration level the maximum splits into two peaks as soon as the temperature cross 0 °C. The spectra were deconvoluted into superpositions of Gaussian and of Lorentzian lines. Typically, resonance frequency of signals from solid (immobilized) protons varies in a random manner, because of randomly distributed local magnetic fields. This phenomenon is characteristic for long molecular correlation times (i.e. very low mobility). It was demonstrated, that in many different solid systems superposition of signals from solid protons represents a single Gaussian line [14]. Conversely, signals from mobile protons (i.e. water molecules) appear in form of Lorentzian lines. These lines usually can be unambiguously separated, what evidence the existence of clearly different proton subsystems. However, in this case, the narrow Lorentzian line may be broadened by the inhomogeneities of external magnetic field, B0.
Fig. 1. Stack plot of the recorded NMR spectra of DNA-DDCA complexes at hydration level (a) 5.0%, (b) 10.1%, (c) 15.6% and (d) 44%.
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The overall surface under line is proportional to the number of resonant nuclei. However in this experiment, it is affected by the sample load and the way the sample powder is compacted inside the test vial. A reliable parameter describing the hydration of the sample is the ratio between the surfaces under Lorentzian and Gaussian line components. All NMR signals for 5.0% sample were satisfactory fitted by the superpositions of one Gaussian line and a single, relatively broad, Lorentzian line component (Fig. 2a). At the hydration level equal 10.1%, it was necessary to consider an additional Lorentzian line at temperatures higher than 20 °C (Fig. 2b) in order to maintain fit quality. At hydration 15.6% and higher, the second Lorentzian line component appeared in the NMR signal even at the lowest temperatures (Fig. 2c). In 15.6% sample line contribution of Lorentzian components were rising with temperature much more rapidly than the contribution of the Gaussian line component. Already at 10 °C the Gaussian line was masked by intense Lorentzian lines and could not be unequivocally fitted. For high hydration levels, it was quite impossible to distinguish a Gaussian component in spectrum of the sample. So, the ratio Lorentzian to Gaussian
line intensities could be further analysed. On the other hand the peak width at half maximum (FWHM) is an intensive parameter, depending on immediate surrounding of proton in the substance. The FWHM is directly related to spin–spin relaxation time T2. Thus, the FWHM can be considered as a reliable probe of water mobility increase due to increasing temperature and/or hydration level. According to FWHM one can assign Lorentzian lines as fingerprints of protons belonging to particular hydration shells. The wider line (L1) results from less mobile protons, i.e. tightly bound water and the narrower one (L2) can be attribute to loosely bound water. The term ‘‘loosely bound water’’ describes water molecules bound via hydrogen bonds to water molecules directly attached to hydrophilic sites on the polymer surface. They are often commonly pictured as secondary and primary shells built over the polymer [35,9]. Thermal dependencies of all the observed L1 line FWHMs evidence two stable states at both extreme ends of temperature range, separated by a transition region. At cryogenic temperatures FWHM of L1 line is very large for all samples, arriving to c.a. 20 kHz at the lowest temperature limit. However, the observed picture is different
Fig. 2. FWHM widths of deconvoluted Gaussian (G) and Lorentzian (L1, L2) lines for DNA-DDCA complexes. Temperature dependence for hydration levels (a) 5.0%, (b) 10.1%, (c) 15.6% and (d) 44%.
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at the opposite temperature limit. With increasing hydration FWHMs stabilize at gradually decreasing values, from 40 kHz in the case of 5% sample to little less than 30 Hz for the most hydrated, 44% sample. The transition region between two stable states, extends from c.a. 20 °C to c.a. +20 °C. However, FWHM behavior is hard to be described there in a consistent manner, common for all samples. The FWHM of L2 behaves somewhat in different way. First of all, at lower hydration and cryogenic temperatures data proceeding good standards do not convince to separate L2 from L1. As it has already mentioned above, the threshold hydration where L2 line emerge, lies between 10.1% and 15.6% hydration levels. Approaching the low temperature end, curves representing L1 and L2 converge, what suggests that at these temperatures there is no more difference between two pools of water. Alternatively, it can be imagined, that initially at very low temperatures exists only tightly bound water (first hydration shell). Next, when temperature rises, some of water molecules are promoted to the second hydration shell, leaving vacancies in the first one (or the overall water accessible surface decreases). The temperature at which L1 and L2 FWHMs diverge, constantly decreases with increased hydration level. At highest hydration levels L1 and L2 components are well separated (i.e. both pools of water) throughout whole temperature range. The stable state of L2 FWHM for all samples settles at high temperatures at 30 Hz and in vicinity of 10 kHz at lowest temperatures investigated. The transition area moves towards lower temperatures with increasing hydration (compare Fig. 2b–d). In case of higher hydrations, definitely above the threshold, L1 and L2 lines with growing temperature constantly converge (see for example Fig. 2d). This phenomenon can be seen as a increasing mobility resulting in fast exchange regime between protons of two hydration shells, what averages their signals, thus, making them indistinguishable.
4. Conclusions According to the literature [35], in the primary hydration shell, at least 11–12 water molecules per nucleotide are in direct contact with DNA. Additional 8–9 water molecules per nucleotide are accommodated indirectly through already bound water molecules. The first hydration shell is completely filled at 80% RH. The experimental results presented above, i.e. two Lorentzian lines identified in the NMR signal, indicate that mobile water fraction exists already at 10.1% RH. This observation can be twofold interpreted. Water molecules that are not in direct contact with DNA, but classically classified as of the first hydration shell contribute to the second Lorentzian line and are part of loosely bound water fraction. In other words, the second hydration shell starts to built up before the primary one is fully filled. Alternatively, it can be assumed that in some parts of the sample (of a different local order for example) the second hydration shells built up starts at a hydration level lower, than believed. Last but not least, water can
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Temperature evolution of hydration shells in solid DNA didecyldimethylammonium chloride complex studied by 1H NMR spectroscopy Jacek Nizioł a,⇑, Piotr Nowak b, Jan Kobierski b, Hubert Haran´czyk b a b
AGH University of Science and Technology, Faculty of Physics and Applied Computer Science, al. Mickiewicza 30, 30-059 Kraków, Poland Jagiellonian University, Institute of Physics, ul. Łojasiewicza 11, 30-348 Kraków, Poland
a r t i c l e
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Article history: Received 18 January 2015 Received in revised form 18 February 2015 Accepted 22 February 2015 Available online 26 February 2015 Keywords: DNA–lipid complex Hydration 1 H NMR spectroscopy Biomaterials Bound water
a b s t r a c t In the case of DNA and its derivatives hydration effect are of paramount importance for many characteristics. Despite years of extensive research this phenomenon is not completely understood yet. A model DNA–lipid complex with didecyldimethylammonium chloride was subjected to gaseous phase hydration procedure. Using 1H NMR spectroscopy a qualitative change in hydration pattern was identified when the material was conditioned in atmosphere of 10.1% of relative humidity. At the threshold hydration level on the top of the first hydration shell appear water molecules that may be attributed to the second hydration shell. This value is lower, that cited in the bibliography as the saturation point of the first hydration level. Ó 2015 Elsevier Ltd. All rights reserved.
Deoxyribonucleic acid (DNA) is a vehicle carrying genetic information, thus since its discovery, it is most frequently discussed as mainly responsible for the mystery of life. However, from the chemical point of view, DNA is only a biopolymer with very particular and rare properties, resulting from its ‘‘intelligent’’ structure. DNA is a polynucleotide chain consisting of alternating phosphate units monosaccharide (deoxyribose) with bound one of four possible heterocyclic bases. Stable hydrogen bonds occur exclusively between base pairs adenine–thymine and guanine–cytosine. Thus, two single DNA strands of opposite base sequences can bind each to other forming a double stranded helix [26]. Strong affinity to water is inherent property of biomaterials, and in particular of DNA. The native DNA contains a significant amount of bound water. Water is not equally distributed within the DNA helix. There exist a continuum
⇑ Corresponding author. E-mail address: [email protected] (J. Nizioł). http://dx.doi.org/10.1016/j.eurpolymj.2015.02.037 0014-3057/Ó 2015 Elsevier Ltd. All rights reserved.
of states represented by water molecules hydrating chemically compatible sites on the helix surface. It has been widely accepted for a long time [35] an intuitive, simplified description of DNA hydration in terms of discrete hydration shells, the primary and the secondary one. Infrared spectroscopy provided evidence that completely filled primary shell consists of about 20 water molecules per nucleotide (wpn). It is achieved in equilibrium with the surrounding atmosphere at least 80% of relative humidity (RH). Water molecules in the primary shell differ in properties from bulk water. These molecules do not form ice crystallites even at temperatures well below 0 °C [8,25]. They are tightly bound and are essential to ensure stability of DNA microstructure [5]. Thus, it is virtually impossible to entirely remove water from DNA [43]. Water in the second hydration shell can be hardly distinguish from the bulk water [46]. The most important secondary conformations of DNA molecule, are referenced to as right-handed double-helical forms of the type A, B, C, D, and the left handed double-helical Z form. At room temperature, and at >90% RH solid
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DNA adopts B conformation. Upon dehydration form B undergoes some conformational transitions (to e.g. A or C form) depending on bases sequence, bound counterions, and other environmental conditions [46,45]. Extreme dehydration introduces a disordered state of DNA, which is characterized by a collapse of base stacking [49,37,20]. The rehydration process reverts these changes [7,49]. Dehydration is accompanied by a two-step decrease in conductivity of DNA samples [44]. Theoretical simulations indicate percolation within hydrogen-bonded water molecule network on DNA surface as the origin of critical phenomena related to hydration [3]. Organic electronics and photonics need materials in form of solid thin films of micron or of submicron thickness. Such films prepared from DNA derivatives combine unique optical and electronic properties [10]. Polymeric materials are typically processed into thin films through a variety of solution based techniques. In its natural environment, in every living cell, DNA exists in aqueous medium. Water evaporates slowly and it has high surface tension. This makes water difficult as the solvent for routine processing of polymeric materials. The natural water-soluble DNA-Na + salt can be treated with an amphiphilic cationic surfactant, to obtain complex that is insoluble in water but soluble in organic solvents, as alcohols [32]. It was shown that the cationic surfactants cooperatively bind to negatively charged DNA molecules in dilute solutions [23]. Stiffness differs the DNA molecule from majority of synthetic polymers. DNA double helix is a rigid cylinder with a diameter of about 2 nm and with persistence length of more than 30 nm [26]. Therefore, it cannot be wrapped easily around the surfactant micelles as in the case of synthetic polymers. DNA–surfactant complexes condensate to a compact, dense form [24] which may adopt lamellar or inverted hexagonal structure [18,2]. Overall properties of DNA and DNA–surfactant complexes in solid form very much differ from the long-time studied DNA dissolved in water [29]. Thin films from DNA–lipid complexes can be prepared either on substrates or as free standings. The choice of surfactant molecule determines mechanical properties of the free standing films, that can be brittle [22] or enough elastic to be stretch orientated [31]. At present, derivatives of DNA and different surfactants are considered as interesting material for a variety of applications. There are many reports on fully functional devices like organic light emitting diodes (OLED) [13,40,11], organic field effect transistors (OFET) [39,33], fuel cells [21,34], or lasers [48]. Extensive research concerning DNA based materials is also carried out in the field of nonlinear optics [27,36,41,42]. Lipid-based DNA formulations are also extensively studied in biochemistry and medicine for applications in modern gene therapy [47] and for pharmaceuticals administration [4]. However, there is still running debate how far DNA condensed with a cationic surfactant retains affinity to water, however significantly weaker. For example, in the case of the most extensively investigated DNA complex with hexadecyltrimetyl ammonium chloride (CTMA), at 80% RH materials’ moisture uptake attains about half of the value for native DNA [19,16]. Nevertheless, little is known about the behavior of the
complexes at low hydration form. Temporally stable properties of devices including a DNA–surfactant complex cannot be achieved without this knowledge. In our previous papers [15,30] we presented a hydration kinetics of a model complex of DNA and didecyldimethyl-ammonium chloride (DDCA), studied by 1H NMR spectroscopy. In the NMR signal we identified three component distinctly different in molecular mobility, manifesting as different values of relaxation times T⁄2 (spin–spin), and T1 (spin–lattice). These components were assigned to the solid state fraction and water from two hydration shells. Surprisingly, signal from the mobile water fraction appeared already at relatively low hydrations. The mass uptake at the threshold corresponded to c.a. 4–5 water molecules per nucleotide. In the current work we studied samples at increasing hydrations surrounding this threshold value. The research was enlarged by including thermal evolution of hydration depended variation of spin–spin relaxation. We believe that this approach yields a more precise insight into water dynamics at the critical hydration level. 1. Materials DNA extracted from salmon milt and roe was purchased from CIST (Chitose Institute of Science and Technology, Japan). DNA complex was prepared using double didecyldimethylammonium chloride (DDCA), an amphiphilic lipid consisting of cationic quaternary ammonia ‘‘head’’ and two alkyl ‘‘tails’’. The synthesis was based on simple ion-exchange reaction and has already been described in details elsewhere [28]. The obtained material was dried in ambient conditions and grinded in agate mortar into a fine powder. 2. Experimental DNA and its derivatives have natural affinity for water, to the extent that often water is considered as an inseparable constituent of DNA [35]. Therefore, the ‘‘dry mass’’ strongly depends on experimental procedure used for determination. To our best knowledge, any method is widely accepted as a standard procedure. It is known that heat [17] and vacuum [1] may irreversibly modify DNA microstructure. Disintegration of DNA complexes to low molecular mass compounds occurs at temperatures as high as above 200 °C [28]. From the other side, the exact kinetics and mechanisms involved in dehydration of DNA complexes are still unclear. Thus, excessive heating causes risk for the sample microstructure which can be irreversibly modified, even though the chemical composition is still unchanged. Therefore we suggest our standard DNA dehydration mode as follows. At first, the sample is stored in a desiccator over silica-gel. As soon as the mass of the sample reached a constant value, the sample is transferred into a vacuum dryer and stored there at 70° for 12 h. In result, the ‘‘silica-gel dry’’ DNA-DDCA sample loses c.a. 7.5% of its mass. At 70 °C DNA complexes are thermally stable, as proved by IR spectroscopy and by X-ray diffractometry [28,38]. In many 1H NMR experiments involving ‘‘dry’’
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DNA complexes, dried according to different protocols, we detected only one broad Gaussian line. Such a line is usually assigned to immobilized protons of the solid phase. Therefore, we prefer to define hydration level in terms of RH of the incubation atmosphere, where initially ‘‘dry’’ sample is stored as long as constant mass is reached. This approach seems more reasonable than at first claim a value to be the ‘‘true’’ dry mass and next, after hydration procedure, calculate water uptake. Controlled hydration of the samples was achieved by incubation in desiccators, over saturated aqueous salt solutions. The chosen series of solution provided relative humidity (RH) from 5% to 44%. A preliminary research suggested a qualitative breakthrough in DNA-DDCA hydration pattern within these range. RH values are used in the further text as references for samples. 1 H NMR spectra were collected using Bruker Avance III spectrometer with p/2 pulse series. The spectrometer was equipped with a thermo-controlled sample compartment and superconducting magnet providing magnetic field B0 = 7 T. The resonance frequency for protons was 300.13 MHz, the p/2 pulse duration 2.2 ls, the repetition rate 2 s and the power 400 W. To eliminate error due to statistically occurring material differences, all experiments were performed using the same DNA-DDCA sample. After each experimental series, the sample was dehydrated then hydrated to a next, higher level. NMR spectra were collected at temperatures decreased from the ambient to 55 °C, then raised, to avoid premature denaturation, to not more than 70 °C. Spectra recorded at cryogenic temperatures were identical regardless the direction of the temperature course.
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Independently, it was verified that the recorded signal pattern did not vary below 55 °C.
3. Results and discussions A distinct visual difference of the recorded NMR spectra is observed as hydration level increases. Exemplary stack plots of NMR signals are presented in Fig. 1. For the sake of space economy, in this figure are shown exclusively signals for extreme hydration levels (5% and 44%) and for two hydration levels (10.1% and 15.6%), where a threshold transition occurs. In Fig. 1(b) for 10.1% hydration level, spectra are featureless across entire temperature span, while in the next Fig. 1(c) for 15.6% hydration level the maximum splits into two peaks as soon as the temperature cross 0 °C. The spectra were deconvoluted into superpositions of Gaussian and of Lorentzian lines. Typically, resonance frequency of signals from solid (immobilized) protons varies in a random manner, because of randomly distributed local magnetic fields. This phenomenon is characteristic for long molecular correlation times (i.e. very low mobility). It was demonstrated, that in many different solid systems superposition of signals from solid protons represents a single Gaussian line [14]. Conversely, signals from mobile protons (i.e. water molecules) appear in form of Lorentzian lines. These lines usually can be unambiguously separated, what evidence the existence of clearly different proton subsystems. However, in this case, the narrow Lorentzian line may be broadened by the inhomogeneities of external magnetic field, B0.
Fig. 1. Stack plot of the recorded NMR spectra of DNA-DDCA complexes at hydration level (a) 5.0%, (b) 10.1%, (c) 15.6% and (d) 44%.
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The overall surface under line is proportional to the number of resonant nuclei. However in this experiment, it is affected by the sample load and the way the sample powder is compacted inside the test vial. A reliable parameter describing the hydration of the sample is the ratio between the surfaces under Lorentzian and Gaussian line components. All NMR signals for 5.0% sample were satisfactory fitted by the superpositions of one Gaussian line and a single, relatively broad, Lorentzian line component (Fig. 2a). At the hydration level equal 10.1%, it was necessary to consider an additional Lorentzian line at temperatures higher than 20 °C (Fig. 2b) in order to maintain fit quality. At hydration 15.6% and higher, the second Lorentzian line component appeared in the NMR signal even at the lowest temperatures (Fig. 2c). In 15.6% sample line contribution of Lorentzian components were rising with temperature much more rapidly than the contribution of the Gaussian line component. Already at 10 °C the Gaussian line was masked by intense Lorentzian lines and could not be unequivocally fitted. For high hydration levels, it was quite impossible to distinguish a Gaussian component in spectrum of the sample. So, the ratio Lorentzian to Gaussian
line intensities could be further analysed. On the other hand the peak width at half maximum (FWHM) is an intensive parameter, depending on immediate surrounding of proton in the substance. The FWHM is directly related to spin–spin relaxation time T2. Thus, the FWHM can be considered as a reliable probe of water mobility increase due to increasing temperature and/or hydration level. According to FWHM one can assign Lorentzian lines as fingerprints of protons belonging to particular hydration shells. The wider line (L1) results from less mobile protons, i.e. tightly bound water and the narrower one (L2) can be attribute to loosely bound water. The term ‘‘loosely bound water’’ describes water molecules bound via hydrogen bonds to water molecules directly attached to hydrophilic sites on the polymer surface. They are often commonly pictured as secondary and primary shells built over the polymer [35,9]. Thermal dependencies of all the observed L1 line FWHMs evidence two stable states at both extreme ends of temperature range, separated by a transition region. At cryogenic temperatures FWHM of L1 line is very large for all samples, arriving to c.a. 20 kHz at the lowest temperature limit. However, the observed picture is different
Fig. 2. FWHM widths of deconvoluted Gaussian (G) and Lorentzian (L1, L2) lines for DNA-DDCA complexes. Temperature dependence for hydration levels (a) 5.0%, (b) 10.1%, (c) 15.6% and (d) 44%.
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at the opposite temperature limit. With increasing hydration FWHMs stabilize at gradually decreasing values, from 40 kHz in the case of 5% sample to little less than 30 Hz for the most hydrated, 44% sample. The transition region between two stable states, extends from c.a. 20 °C to c.a. +20 °C. However, FWHM behavior is hard to be described there in a consistent manner, common for all samples. The FWHM of L2 behaves somewhat in different way. First of all, at lower hydration and cryogenic temperatures data proceeding good standards do not convince to separate L2 from L1. As it has already mentioned above, the threshold hydration where L2 line emerge, lies between 10.1% and 15.6% hydration levels. Approaching the low temperature end, curves representing L1 and L2 converge, what suggests that at these temperatures there is no more difference between two pools of water. Alternatively, it can be imagined, that initially at very low temperatures exists only tightly bound water (first hydration shell). Next, when temperature rises, some of water molecules are promoted to the second hydration shell, leaving vacancies in the first one (or the overall water accessible surface decreases). The temperature at which L1 and L2 FWHMs diverge, constantly decreases with increased hydration level. At highest hydration levels L1 and L2 components are well separated (i.e. both pools of water) throughout whole temperature range. The stable state of L2 FWHM for all samples settles at high temperatures at 30 Hz and in vicinity of 10 kHz at lowest temperatures investigated. The transition area moves towards lower temperatures with increasing hydration (compare Fig. 2b–d). In case of higher hydrations, definitely above the threshold, L1 and L2 lines with growing temperature constantly converge (see for example Fig. 2d). This phenomenon can be seen as a increasing mobility resulting in fast exchange regime between protons of two hydration shells, what averages their signals, thus, making them indistinguishable.
4. Conclusions According to the literature [35], in the primary hydration shell, at least 11–12 water molecules per nucleotide are in direct contact with DNA. Additional 8–9 water molecules per nucleotide are accommodated indirectly through already bound water molecules. The first hydration shell is completely filled at 80% RH. The experimental results presented above, i.e. two Lorentzian lines identified in the NMR signal, indicate that mobile water fraction exists already at 10.1% RH. This observation can be twofold interpreted. Water molecules that are not in direct contact with DNA, but classically classified as of the first hydration shell contribute to the second Lorentzian line and are part of loosely bound water fraction. In other words, the second hydration shell starts to built up before the primary one is fully filled. Alternatively, it can be assumed that in some parts of the sample (of a different local order for example) the second hydration shells built up starts at a hydration level lower, than believed. Last but not least, water can
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