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Interactions of Silver Nanoparticles Formed In Situ on AFM Tips with Supported Lipid Bilayers Xitong Liu Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b01545 • Publication Date (Web): 15 Aug 2018 Downloaded from http://pubs.acs.org on August 17, 2018

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Interactions of Silver Nanoparticles Formed In Situ on AFM Tips with Supported Lipid Bilayers

Revision Submitted to: Langmuir

July 8, 2018

Xitong Liu*†,‡

Department of Environmental Health and Engineering, Johns Hopkins University, Baltimore, Maryland 21218-2686

Present addresses: ‡

Department of Civil and Environmental Engineering, Carnegie Mellon University, 5000 Forbes

Ave., Pittsburgh, Pennsylvania, 15213, United States

* Corresponding author: Xitong Liu, E-mail: [email protected], [email protected]. Phone: +1-412-268-7121.

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ABSTRACT A facile approach to functionalizing atomic force microscopy (AFM) tips with nanoparticles (NPs) will provide exciting opportunities in the field of tip-enhanced vibrational spectroscopy and in probing the interactions between NPs and biological systems. In this study, through successive exposure to polydopamine and AgNO3 solutions, the apex of AFM tips was functionalized with silver nanoparticles (AgNPs). The AgNP-modified AFM tips were used to measure the interaction forces between AgNPs and supported lipid bilayers (SLBs) formed on mica, as well as to probe the penetration of SLBs by AgNPs, with an emphasis on the effect of human serum albumin (HSA) proteins. AgNPs experienced predominantly repulsive forces when approaching SLBs. The presence of HSA resulted in an enhancement in the repulsive interactions between AgNPs and SLBs, likely through steric repulsion. Finally, the forces required for AgNPs to penetrate SLBs were higher in the presence of HSA probably due to the increase in the effective size of the nanoscale protuberances on the AFM tip stemming from the formation of protein coronas around the AgNPs.

Keywords. AFM; Silver Nanoparticle; Lipid Bilayer; Human Serum Albumin; Penetration; Interaction Force; Protein Corona; Polydopamine

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Introduction Since its development by Ducker1 and Butt,2 colloidal probe AFM has been widely adopted as a powerful tool in the studies of surface forces. In this technique, a micrometer-sized sphere is attached to the end of an AFM cantilever typically through manipulating the movement of the cantilever under an optical microscope.1 The resulting colloidal probe allows for the measurement of interaction forces between a sphere and a planar surface of interest, which provide fundamental insights into colloidal phenomena. AFM force measurement using colloidal probes has been applied in probing dispersion, electrostatic, hydrophobic, and hydration forces between surfaces and colloids3,4 as well as in understanding the mechanisms of aggregation of colloids,5 bacterial adhesion to surfaces,6 and the organic fouling of water filtration membranes.7,8 In recent years, nano-sized colloidal probes have attracted heightened research attention due to a variety of reasons. First, AFM tips functionalized with silver or gold NPs can enable tipenhanced vibrational (e.g., Raman) and optical (e.g., second-harmonic generation) spectroscopy which allows for the characterization of interfaces at the nanometer spatial resolution.9-11 Second, the widespread incorporation of metal NPs in consumer products12 and their potential applications in biomedical field (e.g., cancer therapy, targeted drug delivery, and antibacterial coating on medical devices)13-15 have raised concern over their adverse effects on human health. For example, AgNPs have been reported to cause damage to human red blood cells, resulting in the leakage of hemoglobin.16,17 A fundamental understanding of the physicochemical interactions between NPs and biological components (e.g., proteins, phospholipid bilayers) is critical to unveiling the mechanisms for the toxicity of NPs and to guiding safe design of nano-enabled

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consumer products and technologies.18 Such physicochemical interactions at the nano-bio interfaces can be interrogated through the employment of NP-functionalized AFM tips. Due to the resolution limit of optical microscope, the minimum size of the colloidal particle that can be attached to AFM tips through the cantilever-moving technique is ca. 1 µm.19 To circumvent this limitation, alternate techniques have been developed to attach NPs to sharp tips.20 These techniques mainly include two types of approaches: manipulation and attachment of NPs to the tips with the aid of optical tweezers or confocal microscopy,21,22 and in situ deposition of NPs on the tips under electron beam irradiation or evanescent wave illumination.23,24 Nevertheless, the advanced devices required in those approaches may not be readily available, which hampers the generalization of those techniques. As a mimic for the bio-adhesive secreted by mussels, polydopamine (PDA) can coat a variety of surfaces under mild conditions.25 Owing to the abundance of catechol groups in PDA, metal ions can be reduced on the PDA film to result in the formation of metal NPs.25 It is shown herein for the first time that successive exposure of AFM probes to polydopamine and silver nitrate solutions resulted in the formation of AgNPs on the apex of the tips. As a proof-ofconcept application, the AgNP-functionalized tips are used in the measurements of the interaction forces between AgNPs and supported lipid bilayers (SLBs), which have been commonly used as models for cell membranes.26,27 Due to the abundance of human serum albumin (HSA) proteins in human bloodstream and saliva,28 the influence of HSA on the interactions with the AgNP-modified tips and SLBs was also investigated. The findings from the force measurements will have important implications for the assessment of the adverse biological impacts and the efficacy of biomedical application of AgNPs in the presence of biomacromolecular coatings.

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Experimental Section Preparation and Characterization of AgNP-Modified AFM Probes. AFM probes (SNL-10, Bruker) with silicon tips at the end of silicon nitride cantilevers were modified with AgNPs. Figure 1 illustrates the procedures for the modification of the AFM tips with AgNPs. The functionalization of an AFM tip by AgNPs was achieved through the formation of a PDA film on the tip29 and the subsequent reduction of silver ions by PDA to form AgNPs.25,30 First, dopamine hydrochloride powder (0.2 g; Sigma-Aldrich) was dissolved in a 15 mM tris(hydroxymethyl)aminomethane hydrochloride (Tris) buffer at pH 8.5 (Sigma-Aldrich). Under constant agitation, the solution gradually turned dark brown, indicating that dopamine underwent polymerization to form PDA.25 An AFM probe was immersed in the PDA solution 45 min to allow for the formation of a PDA film on the probe.29 Next, the probe was gently placed in a Petri dish containing de-ionized (DI) water (18 MΩ·cm, Millipore) to remove unadsorbed PDA and subsequently placed in another Petri dish containing a freshly prepared 100 or 500 mM AgNO3 solution. The dish was covered with aluminum foil to avoid light exposure. After 16 hours, the AFM probe was gently placed in a Petri dish containing DI water to remove the AgNO3 solution droplets attached to the probe. Finally, the probe was stored in a vacuum desiccator at room temperature until use.

Figure 1. Schematic of the modification of AFM probes with AgNPs on the apex.

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The morphology and surface composition of unmodified silicon tips, tips exposed to PDA only, tips exposed to PDA and 100 mM AgNO3, and tips exposed to PDA and 500 mM AgNO3 (to be referred to as Si, PDA, PDA-Ag-100, and PDA-Ag-500 tips, respectively) were examined with an EOL JSM-6700F field emission scanning electron microscope (FE-SEM, JEOL) coupled with an energy dispersive spectrometer (EDS) at an accelerating voltage of 10 kV. Formation of Supported Lipid Bilayers. Small unilamellar vesicles comprised of zwitterionic 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) were prepared using the extrusion method.31-34 The procedure involves the drying of a DOPC solution in chloroform to form a DOPC film on the bottom of an Erlenmeyer flask, the hydration of the film with a HEPES buffer solution (10 mM HEPES, 150 mM NaCl, 2 mM CaCl2, pH 7.4), and the extrusion of the DOPC solution using a mini-extruder (Avanti Polar Lipids Inc.) through a polycarbonate membrane with a pore size of 50 nm (Whatman) to obtain unilamellar DOPC vesicles. The vesicles were stored at 4 °C and used within seven days after extrusion. DOPC SLBs were then formed on mica through vesicle fusion.26 A freshly cleaved mica (Grade V-1 Muscovite, 2SPI Supplies) was mounted onto the AFM (Multimode NanoScope IIId, Bruker Nano Inc) scanner. An AFM probe with unmodified silicon tips (SNL-10, Bruker) was secured in a glass fluid cell, which was then mounted on the AFM stage. Next, a 50 mg/L DOPC suspension (diluted in HEPES buffer) was slowly injected into the fluid cell with a syringe. After waiting for 10 min to allow for the adsorption of DOPC vesicles and the rupture of the vesicles on mica, tapping-mode AFM imaging was performed to observe the SLBs formed on mica. During the imaging, cantilevers with a nominal spring constant of 0.24 N/m were oscillated at a resonance frequency of ca. 18.5 kHz with a root-mean-square amplitude of 0.5 V.

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AFM Force Measurements. The PDA and PDA-Ag-500 tips were employed in the force measurements with SLBs. All force measurements were carried out at 1 or 150 mM NaCl and pH 7 (buffered with 0.4 mM NaHCO3) at room temperature. The NaCl concentration of 1 and 150 mM were chosen to represent low and high ionic strengths in biological fluids (e.g., saliva versus blood serum35), respectively. After the mica surface was covered mostly by the SLB as revealed by the AFM imaging, the fluid cell was rinsed with either a 1 mM or a 150 mM NaCl solution at pH 7 (buffered with 0.4 mM NaHCO3) to remove the vesicles that did not adsorb on the mica surface. The fluid cell was then taken off the AFM stage, cleaned with ethanol and DI water, and dried with nitrogen gas. Probes with PDA or PDA-Ag-500 tips were mounted in the fluid cell and the fluid cell was mounted back on the AFM stage. Force measurements were taken thereafter in the same electrolyte solution. In order to investigate the influence of HSA on the interactions between AFM tips and SLBs, force measurements were further carried out in the presence of HSA. A 500 mg/L HSA solution at pH 7 in the presence of 1 or 150 mM NaCl was injected into the fluid cell to allow for the adsorption of HSA on AgNPs. The system was equilibrated for 20 min before the force measurements were taken. All force measurements were taken within 2 h after the AFM tips were mounted in the fluid cell. During each force measurement, both approach and retract force curves were recorded by the AFM. A scan rate of 0.498 Hz and ramp size of 0.5 µm were employed, leading to a tip approaching and retracting velocity of 0.498 µm/s. The spring constants of the cantilevers were calibrated using the thermal noise method.36 The cantilever deflection versus sample displacement data was converted to force versus separation data using the method reported by Ducker et al.37 Under each condition, the force measurements were taken at three different

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locations on SLB and ten measurements were taken at each location. The average interaction force, interaction energy, and breakthrough force were calculated from the thirty force profiles. To ensure data reproducibility, two or three different probes were used for force measurements under each solution chemistry condition. All force measurements were completed within three hours after the AgNP-modified probes were immersed in solutions, ensuring that the dissolution of AgNPs (less than 1 nm/day)38 was unimportant over the course of the measurements.

Results and Discussion Reduction of Silver Ions by Polydopamine Results in Formation of AgNPs on AFM Tips. Figure 2a and b show the surface morphology of PDA-Ag-100 and PDA-Ag-500 tips, respectively, obtained through secondary electron (SE) SEM imaging. Nanoparticles with spherical shape were observed on the apex of both tips.

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Figure 2. Secondary electron images of PDA-Ag-100(a) and PDA-Ag-500(b) tips. Backscattered electron images of the respective AgNP-modified tips: (c)PDA-Ag-100 (d)PDA-Ag-500 tips. Backscattered electron images of a bare Si tip and a tip only exposed to PDA are shown in Figure S1.

In order to confirm that the NPs formed on the tip apex were AgNPs, the backscattered electron (BE) images of PDA-Ag tips (Figure 2c and 2d, and Figure S1a in the Supplementary Information, SI) as well as that of Si and PDA tips (Figure S1b and c) were collected. Since heavier elements (i.e., elements with higher atomic numbers) have a stronger ability to backscatter electrons than lighter elements, they appear brighter in the BE images.39 Hence, BE imaging can be used to reveal the contrast of regions with different surface compositions.39 The

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BE images of both Si and PDA tips show featureless surfaces (Figure S1b and c), indicating that the surface compositions of these two tips were uniform. In contrast, bright spots were observed on both PDA-Ag-100 and PDA-Ag-500 tips (Figure 2c and d and S1a). Since silver has a higher atomic number than the composing elements of the Si tip and PDA (C, N, and O), the presence of the bright spots on the tip likely suggests that AgNPs were formed on the tip. In order to further confirm that the bright spots on the tips correspond to AgNPs, EDS analysis was performed on both PDA-Ag-500 and PDA tips. The EDS spectrum obtained from a PDA-Ag-500 tip (Figure S2) shows the presence of silver within those bright spots. In comparison, silver was not detected on the PDA tip (Figure S3). Therefore, the bright spots on the BE images of PDA-Ag tips correspond to AgNPs formed on the tip. Figure S4 shows the SE and BE image three different PDA-Ag-500 tips. AgNPs were observed on all three tips, demonstrating the robustness of this modification method. The formation of AgNPs on PDA film can be attributed to the binding and reduction of Ag+ ions by the catechol groups in PDA.25 Upon reduction of Ag+, clusters of silver metal form on the PDA film as a result of heterogeneous nucleation, and subsequently coalesce to form larger particles.40 The diameter of the NPs on the PDA-Ag-100 tip (40 ± 11 nm, n = 30, Figure 1a) was not significantly different (unpaired two-tailed t test, p > 0.05) from that of the NPs on the PDA-Ag500 tip (44 ± 11 nm, n =30, Figure 1b and S4), as measured using Image J (National Institutes of Health). This observation suggests that the size of AgNPs formed on the AFM tips was not appreciably influenced by the concentration of AgNO3 employed during the modification. Further improvement on the method is required to allow for precise control over the size of AgNPs formed on AFM tips.

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AgNPs Protruding from Tip Apex. Force measurements were first carried out on a mica surface using both Si and PDA tips. The two tips experienced similar forces during approaching the mica surface (Figure S5), suggesting that the PDA film formed on the Si tip was compact and that the fraction of polymer loops and chains extending to the solution was minimal. To prove that AgNPs were protruding from the tip apex, force measurements were carried out using PDA-Ag-500 and PDA tips on two different surfaces, namely, mica and DOPC SLBs, at 1 mM NaCl (Figures 3). The work of adhesion, or the energy required to retract the tips from the surface after contact, was calculated by integrating the total area under the retraction curves.5,42,43 For both surfaces, the work of adhesion measured using PDA and AgNP tips differed significantly (unpaired two-tailed t-test, p < 0.01). Upon being retracted from both surfaces, PDA tips experienced considerably more attractive (or less repulsive) interactions with the surfaces than the AgNP tips did, likely due to the adhesive nature of PDA contributed by the catechol groups.44 Therefore, the AgNPs observed in the SE and BE images were protruding from the apex of the tips as opposed to being embedded in the PDA matrix. The protruding NPs on the tip apex are a prerequisite for AFM force measurements. In force measurements using the NP-modified tips, the protruding NPs ensure that the PDA film on the tip has minimum interference on the measurement of the interactions between NPs and the surfaces of interest.

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Figure 3. (a)Representative force profiles during retraction of PDA and PDA-Ag-500 tips from mica at 1 mM NaCl. (b)Work of adhesion for PDA and PDA-Ag-500 tips during retraction from mica. (c)Representative force profiles during retraction of PDA and PDA-Ag-500 tips from DOPC SLBs at 1 mM NaCl. (d)Work of adhesion for PDA and three different PDA-Ag-500 tips during retraction from SLBs. Positive and negative values indicate attractive and repulsive interactions, respectively. Error bars represent standard deviations, n = 30. Asterisks (*) indicate significant difference (p < 0.01) between PDA and PDA-Ag-500 tips.

This facile modification approach circumvents the current challenges in the manipulation of silver nanoparticles for AFM tip functionalization and offers a new avenue to the preparation of AFM tips functionalized with metal nanoparticles (e.g., copper and gold)25,45 through the reduction of metal ions by PDA. Comparing to existing approaches, this technique does not involve the use of advanced devices (such as optical tweezers) to manipulate NPs. The reduction of silver ions takes place in situ on the PDA-coated tip apex, thus eliminating the need to

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introduce additional reducing agent (such as focused electron beam). These AgNP-functionalized AFM tips can be used in the interaction force measurements between AgNPs and environmentally relevant surfaces (such as silica and biofilms) to better understand the propensity for AgNPs to attach to and to release from these surfaces. They can also be used to probe the nonspecific interactions between AgNPs and biological components such as lipid bilayers and proteins. AgNPs Experienced Repulsive Interactions When Approaching Lipid Bilayers. The interactions between AgNP tips and SLBs were measured to demonstrate the potential applications of the tips in studying nano-bio interfaces. Through AFM imaging, the thickness of the lipid bilayer formed on mica was measured to be ca. 4 nm (Figure 4a and b), consistent to reported thicknesses (ca. 5 nm).47 Figure S6 present ten force curves during the approach of an AgNP tip toward an SLB and when the tip was retracted from the SLB. A representative approach force curve is shown in Figure 4c. Herein separation, S, refers to the distance between the tip and mica substrate underlying the SLB. When the tip was brought to a separation smaller than ca. 5 nm, the tip experienced increasing repulsive force most likely due to the indentation of the lipid bilayer by the tip.48 A jump in the force plot was observed (at S = 3 nm) when the applied force exceeded a threshold, indicating that the tip penetrated the SLB and came into contact with the mica substrate.48-51

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Figure 4. (a)AFM image of a mica surface covered with a DOPC lipid bilayer. Traces 1, 2, 3 indicate transects for three holes within the lipid bilayer. (b)Height profiles of the holes within the bilayer corresponding to traces 1, 2, 3 in panel a. (c)A representative force curve during the approaching of a PDA-Ag-500 tip toward an SLB. Force measurements were conducted at 1 mM NaCl.

The interaction forces between AgNPs and SLBs before contact were first examined. The approach interaction forces between an AgNP and a bilayer are presented as a function of their separation distance, D, in Figure 5. This separation distance, D, was calculated by subtracting the thickness of the bilayer, as determined through AFM imaging, from separation, S. The approach force curve of the PDA-Ag-500 tip differs from that of a PDA probe (Figure S7), again demonstrating that the AgNPs formed on the tip were protruding from the PDA film. Figure 5 shows that AgNPs experienced repulsive forces as they approached the SLBs at both 1 and 150 mM NaCl. Since both AgNPs and DOPC SLBs are negatively charged at pH 7,32,52 this repulsive force can be ascribed, at least in part, to electrical double layer (EDL) repulsion. The interaction force curves were further fitted to Eq. 1:53,54 F = Ae − D /λ

(1)

where F is the interaction force in approach curve, A is a pre-exponential constant, and λ is the decay length. The force curves at 1 and 150 mM NaCl were fitted up to separation D of 20 nm

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and 1–2 nm, respectively (Figure S8), in consideration of the respective long and short ranges for EDL interactions.55,56 The fitted decay lengths at 1 and 150 mM NaCl were ca. 5 and 1 nm, respectively, which are close to the theoretical Debye lengths56 (8 and 1 nm at 1 and 150 mM NaCl, respectively). It is noteworthy that, other than electrostatic repulsion, hydration forces stemming from the orderly packed water molecules around the lipid headgroups may also contribute the measured repulsive forces between AgNPs and SLBs at short separations (< 2 nm).55 Presence of HSA Enhanced Repulsive Interactions between AgNPs and Lipid Bilayers. When HSA was introduced into the background solutions, the magnitude of the repulsive force between AgNPs and SLBs was observed to increase for both 1 and 150 mM NaCl (Figure 5a and b). The interaction force curves in the presence of HSA were also fitted to Eq. 1 (Figure S8). The fitted decay lengths were ca. 7 and 3 nm at 1 and 150 mM NaCl, respectively, which were higher (p < 0.01, unpaired one-tailed t-test) than the decay lengths in the absence of HSA at respective NaCl concentrations (Figure 5a and b inserts). HSA can adsorb on the surface of AgNPs via hydrophobic interaction to form coronas.57 Before the HSA-coated AgNPs come into contact with SLB, the adsorbed HSA molecules are expected to be compressed, which is entropically unfavorable and would give rise to a repulsive steric force (Figure 5c).55 The increase in the decay length in the presence of HSA provides evidence that steric (or electrosteric) repulsion56 was present between HSA-coated AgNPs and SLBs. In their AFM study on the interactions between silica colloids and quartz surfaces, Borkovec and co-workers42 observed a similar increase in decay lengths in the presence of poly(ethylene imine) (PEI) which they attribute to electrosteric repulsions stemming from PEI adsorption.

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Figure 5. Representative approach force curves between PDA-Ag-500 tips and DOPC SLBs at (a)1 mM NaCl and (b)150 mM NaCl in the absence and presence of HSA. Inserts show fitted decay lengths. Error bars represent standard deviations, n = 30. Asterisks (*) indicate significant difference (p < 0.01) between fitted decay lengths in absence and presence of HSA. (c)Proposed effects of protein coronas on the interactions forces between AgNPs and SLBs.

In our previous work, the attachment of citrate-coated AgNPs to DOPC SLBs at neutral pH was considerably inhibited in the presence of HSA.58 Since the presence of HSA did not enhance the negative charge of the AgNPs,58 this decreased attachment is most likely a result of steric (or electrosteric) repulsion contributed by the protein coronas on the NPs. In their study on the biocompatibility of AgNPs, Bhunia et al.59 reported that the hemolysis of red blood cells caused by AgNPs was reduced in the presence of egg protein coronas. The force measurement results suggest that this decrease in hemolytic activity may be attributed in part to the inhibition of the direct contact between the AgNPs and cell membranes. Protein Coronas Increased Breakthrough Forces for Nanoparticle Penetration of Lipid Bilayers. Upon contact with AFM tips, SLBs were penetrated when the force applied on the tips exceeded a threshold. This threshold, known as breakthrough force, can be understood as the maximum force the SLBs can withstand before being penetrated by the tip (Figure 6a).60

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Figure 6b presents the breakthrough forces measured during the approaching of AgNP-tips toward SLBs in the absence and presence of HSA. A notable observation is that the presence of HSA increased the breakthrough forces for both 1 and 150 mM NaCl (Figure 6b and S9).

Figure 6. (A)Representative approach force curves between a PDA-Ag-500 tip and an SLB at 1 mM NaCl in the absence and presence of HSA. (b)Forces required for PDA-Ag-500 tips to penetrate DOPC SLBs in the absence and presence of HSA. Error bars represent standard deviations, n = 30. Asterisks (*) indicate significant difference (p < 0.01) between penetration forces in absence and presence of HSA measured using the same tip. (c)Proposed effects of protein coronas on the forces required for the AgNPs to penetrate SLBs. The formation of protein coronas increased the contact area between AgNPs and the lipid bilayer surface thereby raising the breakthrough forces.

In their study on the penetration of SLBs by AFM tips with different geometries, Angle et al.61 reported that lower breakthrough forces were measured using sharper tips (i.e., tips with smaller radius of curvature). To study the change in the size of AgNPs upon HSA adsorption, citrate-coated AgNPs were synthesized through the Tollens process62 using the procedures reported in previous publication63 (also presented in the SI) and incubated the AgNP suspension with 500 mg/L HSA for 20 min. The average hydrodynamic diameter of AgNPs increased from 57.3 ± 1.8 to 64.2 ± 2.7 (n = 5, p < 0.01 in an unpaired one-tailed t-test) after incubation with

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HSA, likely attributed to the formation of protein coronas with a thickness of ca. 3.5 nm. Hence, the increase in the effective size of the protuberance of the AFM tip is also expected when the protruding AgNPs were exposed to the HSA solution. Such rise in effective nanoparticle size can result in a larger contact area between the AgNPs and lipid bilayers (Figure 6c), thus leading to a higher threshold force to penetrate the SLBs.

Conclusions A novel, facile approach to modifying AFM tips with AgNPs was developed based on the in situ reduction of silver ions by polydopamine. The AgNP-functionalized tips were used for

probing the interactions between AgNPs and lipid bilayers. Bare AgNPs experience repulsive forces when approaching negatively charged lipid bilayers, which are likely of electrostatic nature. The presence of protein coronas gives rise to steric repulsion between AgNPs and SLBs. The observed increase in the threshold force for AgNPs to penetrate lipid membranes in the presence of proteins suggests that the penetration of AgNPs into cells64-66 may be reduced upon formation of biomolecular coronas. Further studies that involve a systematic variation in both protein composition and nanoparticle surface properties67,68 will provide critical insights into the role of protein coronas in regulating nanoparticle-lipid membrane interactions. The findings from this study also suggest that the formation of macromolecular coatings on AgNPs has important implications for their environmental and biological applications. For example, the efficacy of AgNPs in disinfection or cancer cell therapy may be obscured by macromolecular coatings which can alter the interactions between AgNPs and the target moieties.

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ASSOCIATED CONTENT Supporting Information Additional Materials and Methods. Additional SEM imaging and EDS analysis of AFM tips. Additional interaction force curves. Semi-log plots of force curves. Forces required for tips to penetrate SLBs. This material is available free of charge via Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]; [email protected]. Phone: +1-412-268-7121.

Present Address Department of Civil and Environmental Engineering, Carnegie Mellon University, 5000 Forbes Ave., Pittsburgh, Pennsylvania, 15213, United States

Notes The author declares no competing financial interest.

ACKNOWLEDGMENTS This research was supported by the National Science Foundation (CBET-1605815). I greatly acknowledge Dr. Kai Loon Chen (Johns Hopkins University, JHU) for insightful discussions. I am grateful to Dr. Patricia McGuiggan from the Department of Material Science and Engineering (JHU) for the calibration of the spring constants of AFM probes as well as Dr. Kenneth Livi and Bryan Crawford (JHU) for their help with SEM imaging. I am also thankful to John Thornton (Bruker) for his help with AFM imaging. 19


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