Direct Observation of Single-Molecule Stick–Slip Motion in Polyamide

(19−27) This technique provides the length detection with subnanometer precision ... (30−32). To investigate the stick–slip motion of a polymer ...
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Letter Cite This: ACS Macro Lett. 2018, 7, 762−766

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Direct Observation of Single-Molecule Stick−Slip Motion in Polyamide Single Crystals Xiujuan Lyu,† Yu Song,† Wei Feng,‡ and Wenke Zhang*,† †

State Key Laboratory of Supramolecular Structure and Materials, College of Chemistry, and ‡Institute of Atomic and Molecular Physics, Jilin University, Changchun, 130012, China S Supporting Information *

ABSTRACT: Stick−slip is a ubiquitous motion in the hydrogen bonding network, which confers the corresponding materials with excellent toughness and strength. The experimental study of the stick−slip mechanism remains challenging because of the complexity of stress accumulation and release. An ideal system for study of this motion should comprise a defined molecular structure and chain arrangement and strong intermolecular interactions. In this study, we detected the stick−slip motion at the single-molecule level in the hydrogen bonding network of polyamide (PA) single crystals through atomic force microscopy (AFM)-based single-molecule force spectroscopy. Our results show that a stiffer force-loading device can enhance the stick capacity by increasing the fracture force and facilitating stress release. We confirm that the chain rotates while slipping and the slip distance is dependent on the unit structure of the hydrogen bonding network.

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sample system and data analysis. An ideal system for the study of the stick−slip motion in hydrogen bond networks should comprise a well-defined molecular structure and chain arrangement and regular multiple hydrogen bonds. Polyamide (PA) single crystals fulfill the above requirements and are ideal systems for the study of stick−slip motion in condensed materials.28,29 Moreover, our previously established method for single-molecule manipulations of polymer chains in poly(ethylene oxide) single crystals can be used to study the stick− slip motion in PA single crystals.30−32 To investigate the stick−slip motion of a polymer chain in PA single crystals (Figures 1a and S1), we pulled a single PA

ydrogen bonding network is critical for determining the mechanochemistry of cells and the mechanics of individual proteins and assembled fibers by providing orderly, stable cross-linking domains with exceptional mechanical properties.1−9 The hydrogen bonding network features high toughness, particularly because of the cooperative stick−slip motion; this characteristic significantly increases the total dissipated energy through repeated rupture and rebinding of hydrogen bonds.3 The control of stick−slip10−14 motion could alter the toughness of the hydrogen bonding network and engineer the functions of the network-based systems over a broad range of mechanical properties. To effectively control the stick−slip motion, we must understand the mechanism and the factors that can affect such motion. The most effective way to understand the mechanism is the direct measurement/ monitoring of the stick−slip process at the single-molecule level. Theoretical simulations have been used to investigate stick−slip processes and obtain useful information, such as the effect of elasticity of the loading device on the stick−slip motion.3,15−18 However, the stick−slip motion in hydrogenbond-containing condensed materials has not been directly observed/measured experimentally due to difficulties in sample preparation and nanometer scale measurement. The developed single-molecule force spectroscopy (SMFS) can characterize stress response at the nanometer scale with piconewton precision.19−27 This technique provides the length detection with subnanometer precision and has been used to examine the sequence-dependent RNA-protein unbinding as well as the nanoscale polymer friction at the liquid−solid interface.14,21 However, investigating the stick−slip motion at the single-molecule level in condensed hydrogen bond-rich materials remains challenging due to the complexity of the © XXXX American Chemical Society

Figure 1. SMFS experiment on PA 66 and PA 6 single crystals. (a) Schematic of the force-induced unfolding of single PA chain from its single crystal. (b) Typical single-molecule force−extension curves obtained from PA 66. For clarity, the force−extension curves were offsite from trace to trace by 2 nN along the y-axis. Received: May 9, 2018 Accepted: June 4, 2018

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DOI: 10.1021/acsmacrolett.8b00355 ACS Macro Lett. 2018, 7, 762−766

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adjacent small sawtooth peaks (ΔLc1) is ∼1.71 nm, which is similar to the contour length of a repeat unit of PA 66 (1.72 nm). This finding confirms that hydrogen bonds break and reform while shifting approximately one repeat unit (Figure 2b,c). Thus, equally spaced small sawtooth peaks are the most direct/clear representation of the stress−strain response to the stick−slip motion. Our hypothesis can be supported by the result obtained from another PA system, namely, PA 6 (i.e., nylon-6) single crystal. A similar sawtooth containing force− extension curve was obtained on PA 6 single crystal (Figure 2d). The distance between the adjacent big peaks is approximately 12.0 nm, which agrees well with the length increment during the unfolding of one complete fold. However, statistical analysis of the small sawtooth peaks that reside on the major force peak of PA 6 shows two major distributions; the first distribution is located at approximately 0.87 nm, and the other one is located at approximately 1.70 nm (Figure 2e). These two values (0.87 and 1.70 nm) correspond to the length of one and two repeat units of PA 6, respectively. As observed in the crystal structure of PA 6, the hydrogen atom of the N−H group and the oxygen atom of the CO group are alternately arranged along the two sides of the main chain in the hydrogen bonding network. When the polymer chain is shifted by a length of one repeat unit along the pulling direction in a fixed orientation of the polymer chain, the hydrogen bond between the N−H and CO groups will not form. However, our SMFS experiments show that the hydrogen bonds are actually formed. This phenomenon indicates that the polymer fragment being stretched has rotated by 180° to form multiple hydrogen bonds again (Figure 2f). To our knowledge, this finding is the first experimental evidence that the polymer chain being stretched in the crystal phase rotates during slipping to search for the binding sites. The thermal-induced rotation of polymer chain has ever been observed by solid NMR in polyethylene crystals at elevated temperature.36 In our case, during the pulling process the external mechanical energy is input into the polymer stem being stretched and give the stem energy for sliding and rotating. The other length distribution of ∼1.70 nm (Figure 2e) corresponds to the movement of two repeat units along the pulling direction, similar to the case in PA 66. Compared with the length increment of 1.70 nm, the population for the length increment of 0.87 nm is much bigger (see the histogram of ΔLc2 in Figure 2e), indicating that the stick process prefers a short slip distance by the chain rotating motion. These results clearly show the influence of chemical composition on the stick−slip motion in PA systems. The concise representation of the stick−slip motion in the PA system could be due to the homogeneous repeat unit and structure in PA 66 and PA 6 single crystals, which are ideal systems for investigation of the stick−slip process. The number of these small sawtooth peaks on each major peak allows for direct visualized expression of stick capacity. Furthermore, a larger fracture force of ∼1 nN (the first fracture in each big peak in Figures 1 and 2) indicates that the strong fixation provided by the adjacent polymer segments leads to homogeneous shear fracture in the hydrogen bonding network. This result differs from catastrophic fracture that occur in mechanical proteins; in this event, external force of ∼200 pN can initiate deformation, rotation of the strand.6 The precise structure confinement within the crystal and homogeneous shear fracture enable the reformation of multiple hydrogen bonds while shifting one repeat unit. However, the

chain out of the single crystals through atomic force microscopy (AFM)-based SMFS. Figure 1b shows the typical force− extension curves obtained from a PA 66 (i.e., nylon-66) single crystal. Two types of sawtooth peaks (the big and small ones) appear in the force−extension curves, and the small sawtooth peaks reside on each of the big peaks. The gaps in between the adjacent big peaks (ΔLc1) are quite regular. Statistical analysis on the ΔLc1 (estimated using worm-like chain fits, WLC)33−35 produced a value of 12.3 nm (Figure 2a). This value agrees well

Figure 2. (a) Contour length increment (ΔLc1) between the adjacent major peaks of PA 66 estimated using WLC fits. The inset is the histogram of ΔLc1. (b) Close inspection of the small sawtooth peaks on each major peak of PA 66. The inset is the histogram of Δlc1. (c) Schematic of the hydrogen bond change in PA 66 single crystal before and after slipping one repeat unit along the pulling direction. The groups of (CH2)4 and (CH2)6 between adjacent acylamino groups are marked in red and black, respectively. (d) Estimation of the distance (ΔLc2) between the adjacent major sawtooth peaks of the force− extension curve obtained from PA 6 single crystal. (e) Enlarged view of one of the major peaks and statistical analysis of the distance between adjacent small sawtooth peaks (ΔLc2) that reside on the major peak of PA 6 system. (f) Structural representation of changes in the hydrogen bonds before and after slip and rotation in PA 6. The groups of (CH2)5 between adjacent acylamino groups are marked in green. A pulling speed of 2000 nm/s was used to collect the data above.

with the length increment during the unfolding of one complete fold of the PA 66 chain from a 5.8 nm thick single crystal. The ΔLc1 of the pattern can thus serve as a fingerprint for identification of the single-molecule unfolding of PA 66 chain from hydrogen bonding networks. A close inspection of the small sawtooth peaks that reside on the big peak reveals the stick−slip motion of the polymer fragment within the single crystal. The distance between the 763

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small sawtooth peaks on each big peak significantly increases with increasing spring constant of the cantilever (Figure 3a,b). To minimize the effect of the unfolded chain on the stick capacity, the big peaks within an extension of 0−40 nm were selected for statistical analysis. The stiffer cantilever exhibits faster force release speed (kA′B′ > kAB, where kA′B′ and kAB represent the slope of the force-release region; Figure 3b). Statistical analysis shows that the most probable value of small peak number increases from 2 to 5 with the increase of spring constant of AFM cantilever from 40 to 693 pN/nm (Figures 3c and S3). This analysis proves that the stick capacity is enhanced by stiffer cantilever. This result agrees well with our steered molecular dynamic (SMD) simulations on PA66 single crystal (see Figure S4). In addition, we found that the fracture force (that is, the first rupture in each big peak) increases with the increment of spring constants of AFM cantilevers in the range of 40−140 pN/nm, in agreement with the previous theory,38 and then become constant in the range of 140−693 pN/nm due to the similar apparent stiffness of the system in the later case that is dominated by chain elasticity in stiff cantilevers (Figures 3d and S5). Our results also show that the above findings are not affected by the force loading rate (i.e., the pulling speed times the apparent spring constant of the system) under our experimental conditions (Figure S6).38,39 This finding agrees well with our previous SMD simulation result, which shows that the stick−slip motion in PA system is not very sensitive to the pulling velocity (in the range of 2−20 m/s). Only when the stretching velocity reaches 200 m/s, the effect become apparent (the sawtooth pattern become irregular).17 The effect of the length of the unfolded chain (i.e., free chain, Figure 1a) on the stick−slip motion was also investigated by analyzing sawtooth peaks at different extensions. The extension of PA 66 is divided into five regions, and each region has a length of 24 nm (close to the unfolding length of two folds in the PA 66 single crystal). Both the peak number and the fracture force decrease with increasing extension (Figures 3e,f, S7, and S8). We established a model by applying the basic elasticity concepts to describe the effect of loading device (AFM cantilever) and free chain on the stick capacity (Figure 4). After

peak number on each major peak considerably varies, and the maximum number is six for PA 66 (Figure 2b). Considering that the PA 66 single crystal used in the current research has a thickness of ∼5.8 nm, approximately seven repeat units were observed in one complete fold. If multiple hydrogen bonds can reform after the polymer chain being pulled slides one repeat unit length, then the maximum peak number observed should be six. However, the number of small sawtooth peaks that reside on the big ones is generally lower than six (Figures 1b and 3a,b). This result indicates that besides chemical composition, other factors can affect the stick capacity of PA chain in its single crystal.

Figure 3. Cantilever-stiffness and free-chain length dependence of stick capacity. The data obtained from different cantilevers are marked with different colors: 40 pN/nm in red, 140 pN/nm in blue, 417 pN/ nm in orange, 511 pN/nm in green, and 693 pN/nm in purple. (a) Typical single-molecule force−extension curves of PA 66 obtained from different cantilevers (from the top curve to the bottom curve the spring constants of cantilevers increase accordingly). For clarity, the force−extension curves were offsite from trace to trace by 2 nN along the y-axis. (b) Comparison of force-release speed between soft (40 pN/nm, the top red trace) and stiff (693 pN/nm, the bottom purple trace) cantilevers. Effect of cantilever spring constant on (c) most probable peak number and (d) most probable fracture forces of first peak in each major peak. Effect of free-chain length (in between the AFM tip and the crystal surface) on (e) the most probable peak numbers and (f) most probable fracture force of first peak in each major peak in different extension ranges. A pulling speed of 2000 nm/s was used to collect the data above.

According to previous theoretical simulations, the elasticity of external components, including the loading device (AFM cantilever) and the free chain (unfolded chain), can significantly influence the stick capacity.37−40 To experimentally test this hypothesis, we pulled the single PA 66 chain out of its single crystal by using AFM cantilevers with different spring constants. Based on the typical curves (Figures 3a and S2), the number of

Figure 4. Model for predicting the effect of loading device and free chain on the stick capacity. 764

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the polymer materials (especially by affecting the stick−slip motion of the polymer chain in the crystal phase; please see Figure S9 in Supporting Information).

each fracture (FA, FC, and FE), the released chain allows for the stress release in external components, including the loading device and the unfolded chain. The competition between the residual stress (FB and FF) stored in external components and the mechanical stability of the reformed hydrogen bonding network (FC) is critical for the stick capacity. The stiffness of the external components (K) is the key factor in stress release. The stiffness K can be written as 1 1 1 = + K Kcant Kchain

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S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsmacrolett.8b00355. Materials and Method, supplementary force−extension curves, and histograms of SMFS experiments (PDF).

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where Kcant and Kchain represent the stiffness of the AFM cantilever and the polymer chain, respectively. The worm-like chain model34,35 was adopted to describe the free chain elasticity with two different lengths, L1 and L2, before and after slipping the same distance of Lslip (the black solid and dashed traces). The slope of the force-release trace (the red dashed traces) between two WLC curves represents the stiffness of the loading device (AFM cantilever, Kcant). Increasing the stiffness of the AFM cantilever (Kcant(AB) > Kcant(AD)) facilitates the stress release and reduces the residue force (e.g., FB < FD). The stick process occurs only when the residue force becomes smaller than the stability of the reformed hydrogen bond network (e.g., FB < FC). In addition, the Kchain can be expressed as (the differential form of WLC model) Kchain =

−3 k T⎡2⎛ d F (x ) x⎞ 4⎤ = B ⎢ ⎜1 − ⎟ + ⎥ ⎝ ⎠ dx 4Ip ⎣ L L L⎦

ASSOCIATED CONTENT

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Wenke Zhang: 0000-0002-4569-6035 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation of China (21525418, 21474041) and the National Basic Research Program of China (2013CB834503).

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