Micromotors Powered by Enzyme Catalysis - Nano Letters (ACS

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Micromotors Powered by Enzyme Catalysis Krishna Kanti Dey, Xi Zhao, Benjamin M. Tansi, Wilfredo J. MéndezOrtiz, Ubaldo M. Córdova-Figueroa, Ramin Golestanian, and Ayusman Sen Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.5b03935 • Publication Date (Web): 20 Nov 2015 Downloaded from http://pubs.acs.org on November 23, 2015

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Micromotors Powered by Enzyme Catalysis Krishna K. Dey,1 Xi Zhao,1,† Benjamin M. Tansi,1,† Wilfredo J. Méndez-Ortiz,2 Ubaldo M. Córdova-Figueroa2,* Ramin Golestanian,3,* and Ayusman Sen,1,* 1

Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.

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Department of Chemical Engineering, University of Puerto Rico-Mayagüez, Mayagüez, PR 00681, Puerto Rico, USA.

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Rudolf Peierls Centre for Theoretical Physics, University of Oxford, Oxford OX1 3NP, UK.

KEYWORDS: Enzymes, Catalysis, Microparticles, Micromotors, Diffusion, Chemotaxis.

ABSTRACT: Active biocompatible systems are of great current interest for their possible applications in drug or antidote delivery at specific locations. Herein, we report the synthesis and study of self-propelled microparticles powered by enzymatic reactions and their directed movement in substrate concentration gradient. Polystyrene microparticles were functionalized with the enzymes urease and catalase using a biotin-streptavidin linkage procedure. The motion of the enzyme-coated particles was studied in the presence of the respective substrates, using optical microscopy and dynamic light scattering analysis. The diffusion of the particles was found to increase in a substrate concentration dependent manner. The directed chemotactic

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movement of these enzyme-powered motors up the substrate gradient was studied using threeinlet microfluidic channel architecture.

Catalytically-powered synthetic motors that mimic the behavior of biomolecular motors and microorganisms have attracted considerable attention due to their possible applications in nanoscale assembly,1 micro-robotics,2-4 and chemical/biochemical sensing.5-10 In particular, a major incentive for the use of autonomous motors for drug or cargo delivery11,12 is that targeted motion, when compared to passive diffusion, allows faster delivery and the use of less material.13 Important hurdles remain, however, before practical in vivo applications of motors become a reality. First, the motors should move in biological fluids that typically have high ion content. This eliminates motility based on self-electrophoresis or ionic diffusiophoresis mechanisms.14 Second, the micro-transporters must be derived from biocompatible materials and should use fuels that are also biocompatible.12,15 Ideally, the motors should employ enzymes as catalysts and substrates usually present in living systems.16-21 Finally, the most “futuristic” scenario involves the design of populations of synthetic micromotors that have the ability to organize themselves, based on signals from their environment, to perform complex tasks.22 Particularly attractive are designs that allow coordinated movement of particles with different functionalities. Here we demonstrate a general procedure for the fabrication of microparticles powered by enzymatic reactions. In addition, ensembles of active microparticles can be directed by substrate gradients, in principle allowing for cargo delivery at specific locations. Single enzyme molecules have already been reported to undergo enhanced diffusion through substrate turnover to cause their own movement.23-25 Furthermore, they show directional chemotaxis in the presence of a substrate gradient.24-26 We therefore, sought to examine whether enzymes can impart similar enhanced activity and directional drift to micron-size particles when tethered to the latter.


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To examine the enhanced diffusivity of enzyme-coated microparticles in the presence of substrates, 0.79 µm streptavidin-functionalized polystyrene microspheres (Spherotech and Polysciences) were coated with biotinylated urease (from Canavalia ensiformis, Sigma-Aldrich) and catalase (from bovine liver, Sigma-Aldrich), prepared in 10 mM phosphate buffer (for details, see Supporting Information (SI)). These enzymes were selected owing to their robustness and relatively high turnover rates at room temperature (urease: kcat = 2.34 ×104 s -1 , catalase: kcat = 2.12 × 105 s -1 )

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Stock solutions of enzyme coated particles, substrate, and 10 mM

phosphate buffer solution were mixed in calculated proportions and injected in a secure seal hybridization chamber forming a quasi-two dimensional layer of liquid. The plastic chamber was then attached over a glass slide and observed under the microscope. Before recording motion of the suspended particles within the liquid layer, the system was checked for convective flows that can affect the measurements. Particle motion was recorded for a period of 30 s, with a frame rate of 60 s-1. The recorded videos were analyzed for mean square displacements and particle diffusion using codes developed in LabVIEW and Vision Development Module (National Instruments). The mean square displacements calculated at various times were fitted to calculate the particle diffusion in two dimensions (see SI). For catalase coated particles, the diffusion coefficient showed nearly 19% enhancement in the presence of the maximum concentration of H2O2 used in the experiments (11.1 mM). Higher concentrations of H2O2 were not used because of the possibility of formation of O2 bubbles that could affect the measurements. Experiments carried out with particles coated with urease showed similar behavior in the presence of its substrate, urea. Diffusion of urease coated particles was measured in urea solutions of different concentrations and at the highest concentration used (213 mM), particle diffusion increased nearly 22%. Importantly, diffusion of both catalase and urease coated particles increased in a


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substrate concentration dependent manner, indicative of the role of substrate turnover in inducing propulsion to these microparticles. The results are shown in Figure 1.

Figure 1. Diffusion of 0.79 µm (A) catalase and (B) urease coated polymer microspheres in different concentrations of H2O2 and urea respectively. The results shows significant ( p < 0.05 ) enhancement in diffusion of enzyme powered particles in the presence of substrates. For each experiment, six independent measurements (~40 particles in each measurement) were analyzed using LabVIEW and vision development module and their mean and standard deviations are reported. Representative plots of mean-square displacements versus time, which show the enhancement in the (effective) diffusion coefficients are provided in the SI (Figure S2). The enhanced diffusion of enzyme-coated micromotors was further investigated using Dynamic Light Scattering (DLS) particle size analyzer. DLS measures intensity of light scattered by colloidal suspensions as a function of time. The motion of the suspended particles leads to timedependent fluctuations in the scattered light intensity, the characteristic time of which depends on the diffusion coefficient of the particles.27 For spherical particles, the time dependent fluctuation in the scattered light intensity can be fitted to an autocorrelation function to estimate


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the diffusion coefficient D of the particles, which can be related to their hydrodynamic diameter d using Stokes-Einstein relation:

D=

kT 3πη d

[1]

Here, k is Boltzmann’s constant, η is solvent viscosity and T is the solution temperature. Following this principle, we measured the diffusion coefficient distribution of enzymefunctionalized polystyrene particles in the presence and absence of substrates. DLS measurements were carried out with lower concentrations of catalytic particles and substrates to minimize agglomeration of enzyme-coated microspheres (for details, see SI). Particle and substrate solutions were prepared in 10 mM phosphate buffer. For particles coated with urease, the diffusivity distributions were recorded in the presence and absence of 0.5 mM urea, with a total experimental solution of 1 mL. The experiments were all carried out at 25 0C and each measurement involved three successive runs, each involving 15 scans on the average. In the absence of the substrate, the average of three measurements showed a diffusion coefficient distribution peak at 0.55 µm2/s, corresponding to the expected hydrodynamic diameter of the particles. However in the presence of 0.5 mM urea, the diffusion distribution shifted towards higher values, showing enhanced diffusion of the particles following substrate turnover. With time, the distribution returned gradually to the zero substrate value showing completion of the enzymatic reaction. Considering the maximum shift observed, the enhanced diffusion calculated for urease coated beads using DLS was nearly 25%. Similarly for catalase coated microspheres, time dependent shift in the diffusivity distribution profile was observed in the presence of 7.3 µM H2O2. The maximum diffusion enhancement recorded for catalase coated beads was approximately 14%, which is only slightly lower than that measured in optical microscopy.


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Results of DLS measurements are shown in Figure 2. Clearly there is a relatively close agreement between the results obtained using two different techniques: optical microscopy and DLS.

Figure 2. (A) Time dependent shifts in the diffusion profiles of 0.79 µm streptavidinfunctionalized polystyrene microspheres coated with (A) catalase and (B) urease, dispersed in 7.3 µM H2O2 and 0.5 mM urea respectively, estimated using dynamic light scattering particle size analysis. As the reaction proceeds, the peak of the distribution profile returns to the zero substrate value, showing gradual consumption of substrates with time. The distribution curves are smoothened with B-spline fitting in Origin. Enhanced diffusion typically emerges at sufficiently long time scales from a short-time propulsion mechanism that comes from actuation28 or self-phoretic gradients29-31 due to orientational randomization.32 This is, however, not necessary, as orientational randomization of symmetrically actuating systems could also lead to enhanced diffusion despite lack of net propulsion along the body axis.33,34. There are in principle, many mechanisms that can contribute towards the enhanced diffusion of a symmetric enzyme-coated bead, such as phoretic density


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fluctuations,35 stochastic mechanical actuation of the enzyme,36,37 and local and collective heating.38,39 We find that for our experimental systems, the contributions due to phoretic density fluctuations and stochastic mechanical actuation is small.39 However, since reactions catalyzed by catalase and urease are strongly exothermic, the collective heating can be significant, and appears to account for the order of magnitude enhancement in the diffusion coefficient, as well as its dependence on the fuel concentration. To estimate this contribution, we note that there are approximately 108 enzyme-coated particles in the observation chamber, each of which has ~105 enzymes. This amounts to an effective enzyme concentration in the 1 µM range. Though quite dilute, catalase concentrations in this range can lead to a temperature increase of a few degrees, and through the resultant decrease in viscosity, to increase the effective diffusion coefficient in the range of 10-20% (see SI).39 We attempted to measure temperature increase in active urease solutions (1 µM urease and 1 M urea in 10 mM PBS/D2O) using a thermocouple and by NMR spectroscopy employing a methanol thermometer. A maximum of 0.2 K increase in bulk temperature during catalytic turnover was observed. However, these techniques do not allow direct access to local temperature variations as experienced by the enzyme-coated beads. In addition, we note that despite the suggestive order of magnitude estimate, other mechanisms could be contributing significantly to the enhanced diffusion. Clearly further work is needed to test our hypothesis. The observed substrate concentration-dependent enhancement in the diffusion of enzymepowered micromotors encouraged us to investigate their behavior with respect to externally imposed substrate concentration gradients. We used fluorescent streptavidin-functionalized polystyrene particles of diameter 2 µm (Fluoresbrite® YG Microspheres, Polysciences, ex/em = 441/486), coated uniformly with biotinylated catalase and urease and allowed the particle


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dispersion to flow through the center of a three-inlet microfluidic architecture. Details of microfluidic channel fabrication are provided in the SI (schematic shown in Figure 3A). Either buffer (control) or the appropriate substrate solution was allowed to flow through the side channels. Enhanced chemotactic shifts of the micromotors in response to substrate gradients when comparted to simple diffusive spread in the buffer solution were measured at specific positions along the length of the channel. The fluorescence intensity was always measured across the channel width, leaving approximately 15 µm from either ends, close to the channel walls. This was done to minimize the effect of background fluorescence of the PDMS wall on the recorded signal.40 The microfluidic device was fabricated following standard soft lithography protocols reported in literature (for details, see SI).41-42 For chemotaxis of urease motors, a solution of enzyme-coated fluorescent microspheres was introduced through the center of the three-inlet device with a flow speed of 50 µL/h. Through the adjacent inlets, solution of either 10 or 100 mM urea prepared in 10 mM phosphate buffer or simply 10 mM buffer without urea (control) was introduced at the same flow rate. After the system attained steady state, sustained concentration gradients of substrate were formed across the interface of the laminar flows. The urease-coated particles, upon interacting with urea concentration gradient displayed chemotactic drift towards regions of higher substrate concentrations. The drift can be quantified by monitoring the normalized fluorescent intensity profile of the particles across the width of the microchannel using a confocal microscope at specific positions along the length of the microchannel. In our experiments, we usually measured and compared the shifts at 38 mm away from the start of the inlets. As shown in Figure 3(B), there is a greater spreading of the particles when urea rather than buffer alone is present in both the flanking channels. When urea is introduced into one side channel and buffer only in the


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other, there is a clear preferential spreading of the particles towards the urea containing channel (Figure 3(D)).


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Figure 3. (A) Schematic of the three-inlet microfluidic set up used to observe chemotaxis of enzyme coated particles towards higher substrate concentrations. The excess migration of the functionalized particles towards the substrate side was quantified by measuring the fluorescence intensity of the polymer spheres along a straight line across the channel (shown in red) at a distance of 38 mm from the start. The figure also shows chemotactic migration of (B, D) urease and (C, E) catalase coated fluorescent microspheres in presence of imposed substrate concentration gradients, observed within three-inlet microfluidic channels. The enzyme functionalized particles are allowed to flow through the middle channel of the device, while through the side channels, either buffer alone or buffered solution of appropriate substrates are introduced at the same flow rate. Figure 3(C) shows greater spreading of catalase coated fluorescent microspheres in the presence of 1 mM H2O2, flowing through the flanking channels compared to buffer alone. The flow speed of liquid through the inlets was maintained at 100 µL/h. Lower H2O2 concentration and higher flow rate was employed to minimize the formation of oxygen bubbles within the microfluidic channel during the measurements and resulting distortion of flow profiles. Experiments performed with substrate and phosphate buffer alone flowing through the side channels simultaneously showed preferential migration of the particles towards the substrate side (Figure 3(E)). Note that due to particle settling, the intensity profiles are different in different z-planes along the depth of the microfluidic channel. For each set of measurements, signals were recorded at the same z-plane under identical conditions. By measuring the chemotactic shift at different positions in the microfluidic channel along its length, the magnitude of the shift as a function of time was obtained for urease-coated particles. For laminar flows of liquid under steady state conditions, different positions along the length of


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the microchannel will correspond to different interaction times for the enzyme coated particles with the imposed substrate concentration gradients. This allows us to correlate the chemotactic shift with the duration of the substrate-particle interaction (defined as the reaction time). As shown in Figure 4A, the chemotactic shift of particles towards the substrate side increases linearly with reaction time for constant concentration of substrate at the inlet (10 mM urea for urease coated microparticles). Also, as shown in Figure 4B, for increased concentration gradient of urea (obtained by increasing urea concentration at the inlet), magnitude of chemotactic shifts can also be increased. These results demonstrate that substrate catalysis by enzymes anchored to a particle surface lead not only to their directional migration along the substrate gradient, but the extent of the migration can also be controlled by changing either the substrate-particle interaction times or the concentration of substrate at the inlet.

Figure 4. Chemotactic migrations of urease coated microparticles measured at different times (at different positions of the microfluidic channel along its length, from the start) at (A) 10 mM and (B) 100 mM urea. The error bars represent standard deviations for six independent measurements.


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In summary, we have demonstrated that enzymatic reactions may be utilized to power micronsized polymer particles in solution. In addition, these hybrid micromotors can respond to specific chemical signals by moving directionally towards specific regions in space. The results constitute the first steps in the fabrication biocompatible, multifunctional hybrid motors for carrying out specific functions under physiological conditions. ASSOCIATED CONTENT Supporting Information. Details of particle coating with biotinylated enzymes, optical microscope studies, diffusion coefficient calculations using LabVIEW, DLS measurements, estimation of enzyme concentration in the experimental solution and microfluidic channel fabrications are provided as Supporting Information. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Authors *Dr. Ayusman Sen, Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, USA. Email: [email protected] *Dr. Ramin Golestanian, Rudolf Peierls Centre for Theoretical Physics, University of Oxford, Oxford OX1 3NP, UK. Email: [email protected] *Dr. Ubaldo M. Córdova-Figueroa, Department of Chemical Engineering, University of Puerto Rico-Mayagüez, Mayagüez, PR 00681, Puerto Rico, USA. Email: [email protected] Author Contributions


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The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. †These authors contributed equally. ACKNOWLEDGMENT We thank Penn State MRSEC under NSF grant DMR-1420620 for financial supports. UMCF acknowledges NSF CAREER award no. CBET-1055284 for funds. We thank Dr. Stephen Ebbens and Dr. Jonathan Howse from University of Sheffield for providing us the LabVIEW codes for MSD analysis. We also acknowledge Penn State Materials Characterization Laboratory for providing access to Dynamic Light Scattering Measurement Facilities.


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13. Brangwynne, C. P.; Koenderink, G. H.; MacKintosh, F. C.; Weitz, D. A. Trends Cell Biol 2009, 19, 423-427. 14. Wang, W.; Duan, W.; Ahmed, S.; Mallouk, T. E.; Sen, A. Nano Today 2013, 8, 531-554. 15. Zhang, H.; Duan, W.; Liu, L.; Sen, A. J. Am. Chem. Soc. 2013, 135, 15734-15737. 16. Peng, F.; Tu, Y.; van Hest, J. C. M.; Wilson, D. A. Angew. Chem., Int. Ed. 2015, 54, 11662-11665. 17. Mano, N.; Heller, A. J. Am. Chem. Soc. 2005, 127, 11574-11575. 18. Gáspár, S. Nanoscale 2014, 6, 7757-7763. 19. Ma, X.; Jannasch, A.; Albrecht, U-R.; Hahn, K.; Miguel-López, A.; Schäffer, E.; Sánchez, S. Nano Lett. 2015, 15, 7043-7050. 20. Bunea, A-I.; Pavel, I-A.; Davis, S.; Gáspár, S. Chem. Commun. 2013, 49, 8803-8805. 21. Pavel, I-A.; Bunea, A-I.; David, S.; Gáspár, S. Chem. Cat. Chem. 2014, 6, 866-872. 22. Duan, W.; Liu, R.; Sen, A. J. Am. Chem. Soc. 2013, 135, 1280-1283. 23. Muddana, H. S.; Sengupta, S.; Mallouk, T. E.; Sen, A.; Butler, P. J. J. Am. Chem. Soc. 2010, 132, 2110-2111. 24. Sengupta, S.; Dey, K. K.; Muddana, H. S.; Tabouillot, T.; Ibele, M. E.; Butler, P. J.; Sen, A. J. Am. Chem. Soc. 2013, 135, 1406-1414. 25. Sengupta, S.; Spiering, M. M.; Dey, K. K.; Duan, W.; Patra, D.; Butler, P. J.; Astumian, R. D.; Benkovic, S. J.; Sen, A. ACS Nano 2014, 8, 2410-2418.


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ToC Graphic

Synopsis Enzyme-functionalized microparticles behave as hybrid autonomous motors in appropriate substrate solutions. Diffusion of enzyme-powered micromotors increases in a substrate concentration-dependent manner. In the presence of imposed substrate gradients, the particles show directed chemotactic migration towards regions of higher substrate concentration.


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