Glucose-Fueled Micromotors with Highly Efficient Visible-Light

Jan 23, 2019 - Such motors with outstanding propulsion in biological environments and wireless, repeatable, and light-modulated three-dimensional moti...
0 downloads 0 Views 889KB Size
Subscriber access provided by UNIV OF LOUISIANA

Functional Inorganic Materials and Devices

Glucose-fueled Micromotors with Highly Efficient Visible Light Photocatalytic Propulsion Qinglong Wang, Renfeng Dong, Chun Wang, Shuyu Xu, Decheng Chen, Yuying Liang, Biye Ren, Wei Gao, and Yue-Peng Cai ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b17563 • Publication Date (Web): 23 Jan 2019 Downloaded from http://pubs.acs.org on January 27, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

Glucose-fueled Micromotors with Highly Efficient Visible Light Photocatalytic Propulsion Qinglong Wang,a Renfeng Dong,a* Chun Wang,a Shuyu Xu,a Decheng Chen,a Yuying Liang,a Biye Ren,b Wei Gaoc and Yuepeng Caia* a

School of Chemistry and Environment, Guangzhou Key Laboratory of Materials for Energy

Conversion and Storage, Guangdong Provincial Engineering Technology Research Center for Materials for Energy Conversion and Storage, South China Normal University, Guangzhou 510006, China b

Research Institute of Materials Science, South China University of Technology, Guangzhou

510640, China c

Department of Medical Engineering, Division of Engineering and Applied Science, California

Institute of Technology, Pasadena, California 91125, United States

ABSTRACT: Synthetic micro-nanomotors fueled by glucose are highly desired for numerous practical applications due to the biocompatibility of their required fuel. However, currently all of the glucose-fueled micro/nanomotors are based on enzyme-catalytic driven mechanisms, which usually suffer from strict operation conditions and weak propulsion characteristics that greatly limit their applications. Here, we report a highly efficient glucose-fueled cuprous oxide@N doped carbon nanotube (Cu2O@N-CNT) micromotor, which can be activated by environment-friendly visible light photocatalysis. The speeds of such Cu2O@N-CNT micromotors can reach up to 18.71 m/s, which is comparable to conventional Pt-based catalytic Janus micromotors usually fueled by toxic H2O2 fuel. In addition, the velocities of such motors can be efficiently regulated by multiple approaches, such as adjusting the N-CNT content within the micromotors, glucose concentrations, or light intensities. Furthermore, the Cu2O@N-CNTs micromotors exhibit highly

ACS Paragon Plus Environment

1

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 16

controllable negative phototaxis behavior (moving away from light sources). Such motors with outstanding propulsion in biological environments, and wireless, repeatable, light-modulated three-dimensional motion control are extremely attractive for future practical applications. KEYWORDS: micromotors, glucose, visible light, Cu2O, N-CNTs INTRODUCTION

Artificial micro/nanomotors are tiny objects that can autonomously move under the influence of an appropriate source of energy, such as chemical fuels,1, 2 magnetic field,3, 4 electrical field,5, 6 ultrasound,7,

8

or light9,

10

etc, and hold considerable promise for diverse future applications.

Catalytic nanomotors are one of the most attractive types of micro/nanomotors which can convert local chemical fuel in solution into mechanical work, and they exhibit outstanding potentials in various fields, ranging from environmental remediation11,

12

to biomedical applications.13,

14

However, most self-propelled systems reported so far, such as metallic nanowires,15,

16

microtubular microrockets,17, 18 Janus micro-spheres,19, 20 and supermolecule-based nanomotors,21, 22

require toxic chemical fuels (H2O2, I2, Br2, N2H4), greatly limiting their practical applications.

As a result, efficiently operating artificial micro/nanomotors with biocompatible fuels in order to broaden their practical applications is still a great challenge in nanotechnology. Glucose, abundantly present in biological environments, could be an ideal biocompatible fuel candidate. However, all of the glucose-fueled micro/nanomotors reported previously are powered by enzymecatalyzed glucose oxidation, which usually requires strict operation conditions and exhibits weak propulsion.23, 24 Therefore, in order to expand the applications of glucose-fueled micromotors, improving their propulsion has become critically important. Photocatalytic decomposition of glucose is an important and efficient approach which has been widely used in various glucose-related research, including biosensors,25 hydrogen evolution,26 and self-monitoring of blood glucose.27 In light of this, we propose using photocatalytic reactions instead of enzyme-catalytic reactions to decompose glucose and further convert the chemical energy of glucose to mechanical energy of micro/nanomotors. Considering the balance between maintaining a biocompatible operation environment and the efficient propulsion of micro/nanomotors, visible light is the best choice as the activated condition. Cu2O is a well-known photocatalyst with excellent photocatalytic activity. Owing to its narrow band gap

ACS Paragon Plus Environment

2

Page 3 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

of 2.17 eV, it can be activated under visible light (700 nm),28 making it an ideal material for the photocatalytic degradation of glucose. In general, under visible light, charge separation is generated within Cu2O, and since the electrons are in an unstable state, they easily recombine with holes, which reduces the photocatalytic activity of Cu2O. In light of this, we choose nitrogen-doped carbon nanotubes (N-CNTs) to solve this deficiency of plain Cu2O. A classic carbon material with immense importance owing to its excellent electrical properties, N-CNTs have been widely applied in energy and catalysis.29 By doping N-CNTs into photocatalysts, carbonaceous species are formed on the surface of photocatalyst, which facilitate electron transfer and greatly reduce the charge recombination, thus further improving the photocatalytic efficiency.30 As a result, N-CNTs doped Cu2O shows great potential for preparing microrobots based on the clean energy sources of visible light and glucose and for improving the propulsion of such motors. In this paper, we propose an excellent micromotor based on Cu2O@N-CNTs driven by the photocatalytic reaction of glucose. These new Cu2O@N-CNTs micromotors display efficient propulsion (as high as 18

m/s) in a fully green environment: a glucose solution under visible

light (Figure 1A). Under the same light illumination, such photocatalytic micromotors exhibit substantially more efficient proplusion in a glucose evironment than that without glucose fuel (Figure 1B and C). In general, most of chemical fuels which can give micro/nanomotors strong propulsion are usually highly toxic, however, biocompatible fuels usually generate weak propulsion for micro/nanomotors.31 This work is the first to demonstrate that glucose-fueled

Figure 1. (A) Schematic of the Cu2O@N-CNTs spherical micromotor in a glucose solution under green light. (B) The trajectory over 3 seconds of Cu2O@N-CNTs micromotors without glucose and (C) after adding 20 mM glucose respectively under visible green light (taken from Video S1). Scale bar: 10 m

ACS Paragon Plus Environment

3

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 4 of 16

micromotors can also exhibit efficient propulsion comparable with that of classic Pt-based Janus catalytic micromotors fueled by toxic H2O2.32 In addition, it is also the first demonstration of using photocatalytic decomposition of glucose to efficiently propel micro/nanomotors. Unlike previously reported glucose oxidase-based micro/nanomotors, these outstanding Cu2O@N-CNTs micromotors with attractive photocatalytic propulsion, simple preparation procedures, fully green energy requirement and tunable light-controlled characteristics hold great potential for future practical applications. EXPERIMENTAL SECTION Synthesis of Cu2O@N-CNTs micromotor. The synthesis of N-CNTs was based on previous reports33, 34 and 0.012g of N-CNTs was dispersed in 100 ml of ethanol (Damao Chemical Reagent Factory) and ultrasonically pretreated for 24 hours. 0.2g copper acetate (Aladdin #C105398) and 0.4g SDS (Acros #151-21-3) were added into a round bottom flask with 8ml water, followed by addition of 2.5, 4.2, 5.8, 7.5 ml of ethanol dispersion containing N-CNTsand 5.5, 3.8, 2.2, 0.5 ml of ethanol, respectively. In the oil bath, when the temperature reached 73 °C, 0.28 g of sodium hydroxide (Tianjin ZhiYuan Reagent Co, Ltd) and 0.24 g of glucose (RichJoint Chemical) were added, and the reaction was carried out for 30 minutes. The resulting brick red precipitate was washed with DI water (18.2 MΩ·cm) for 5 times, and dried at 60 °C in vacuum. Finally, Cu2O@NCNTs micromotor (diameter: 1 to 1.5 µm) were obtained. Motion calibration experiments. To determine the relationship between the active motion of Cu2O@N-CNTs micromotor and light, we used the ND Filter in the microscope (4 X, 8 X, 16 X) to control the illumination intensity. The light illumination intensity here has 4 levels: 55300 Lux, 13810 Lux, 6500 Lux, and 3170 Lux. 100 Lux is background light. The wavelength of green light ranges from 510560 nm, and the wavelength of blue light is 450490 nm. In this system, videos were all recorded with the 40X objective and the number of samples per experiment was 30. The average velocity was calculated and the entire procedure was repeated six times. The trajectories of each individual particle were tracked by using the NIS-Elements AR 4.3 software. A typical video is captured with 30 frames per second. The analysis software compares and tracks the displacement of each particle on a frame-by-frame basis. After obtaining the tracking trajectories

ACS Paragon Plus Environment

4

Page 5 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

for each micromotors, the mean square displacement (MSD) after the fixed time interval Δt is calculated by the following formula (1): (MSD)|(Δt) = ⟨(x(Δt)-x0)2+(y(Δt)-y0)2⟩

(1)

The angle brackets ⟨•⟩ indicate that we calculated the average MSD of 30 particles, and the original position of the motor is indicated by the subscript "0", and the particle coordinates in the plane of motion after the time interval Δt are represented by x(Δt) and y(Δt). The result allows us to accurately determine the Brownian particle displacement or mean square displacement (MSD) of every particle. The propulsion calibration experiments were performed by mixing 2 µL of the motors dispersed in deionized water. Equipment. XRD patterns were obtained by X-Ray Diffractomer (Bruker D8 Advance, Germany), SEM patterns were obtained by Tescan MAIA 3. XPS analyses were performed using X-ray photoelectron spectrometer (Escalab 250xi, United States). The analysis of TG was obtained by Thermal Gravimetric Analyzer (Netzsch TG 209 F1 Libra, Germany). Visible light was generated by Mercury lamp sockets and dichroic mirror DM 400. Barrier filter BA520 was used to generate blue light and barrier filter BA590 for green light. Illumination intensities were controlled by ND filters (4×, 8×, 16×) (all from Nikon). Videos were captured by an inverted optical microscope (Nikon Instrument Inc. Ti-S/L100), coupled with 40× objectives, and a Hamamatsu ORCA-flash 4.0 LT (C11440) sCMOS digital camera using the NIS-Elements AR 4.3 software. All the illumination intensities were calculated by TASI digital light meter TA8120. RESULTS AND DISCUSSION The Cu2O@N-CNTs micromotors are simply prepared by a one-pot method which is repeatable and suitable for mass production. Briefly, in a certain ratio, N-CNTs, copper acetate, SDS, sodium hydroxide and glucose are dissolved in an ethanol aqueous solution. The reaction is carried out for 30 minutes at 73 °C, and the micro-motors are obtained after washing with DI water for 5 times and drying at 60 °C in vacuum. The structure of Cu2O@N-CNTs micromotors are well characterized by scanning electron microscope (SEM). As the content of N-CNTs increases, more N-CNTs composites were interspersed within the motor. The SEM images of the motors with different N-CNTs content ( 0%, 0.91%, 1.72%, and 2.35%)

are shown in the Supporting

Information. As shown in Figure 2A N-CNTs are well complexed and interspersed in Cu2O

ACS Paragon Plus Environment

5

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 6 of 16

microsphere. X-ray diffraction (XRD) patterns (Figure 2B) further confirm that the motor has highly crystalline Cu2O, and inserted SEM image confirms that the particle size distribution of the Cu2O@N-CNTs micromotor is uniform and the diameter is about 1.5 m. It is worth noting that due to the low content of N-CNTs, no obviously corresponding characteristic peaks are observed in XRD results. However, the existence of N-CNTs has been solidly confirmed by SEM and Xray photoelectron spectroscopy (XPS). Detailed XPS analysis of the characterization is described in the Supporting Information.

Figure 2. (A) SEM image of single Cu2O@N-CNTs composite micromotor with 1.35% N-CNTs content. (B) X-ray Diffraction (XRD) pattern of the Cu2O@N-CNTs micromotors and the inset is SEM image of multiple Cu2O@N-CNTs micromotors with 1.35% N-CNTs content.

In this system, we have built asymmetric surface chemical reactions on Cu2O@N-CNTs particles by the limited penetration depth of light in the as-prepared materials, The products of the photoinduced reaction are mainly released from the irradiated side of the particles, thereby producing a net product concentration gradient around the particles, further providing the driving force for directional propulsion of the motor. The detailed process is schematically illustrated in Figure 3A: upon exposure to visible light irradiation on one side of the micromotors, charge separation occurs within the Cu2O, causing electrons to migrate from the Cu2O conduction band to the N-CNTs. The presence of N-CNTs greatly hinders the charge recombination, which leads to strong photocatalytic activity. All the holes and the charges participate in the glucose photocatalytic decomposition reaction cycles, forming a product gradient around the motors surface, which further propels the micromotors. According to the photocatalytic mechanisms of classic metal oxide photocatalysts, the detailed reactions in such systems have been described in

ACS Paragon Plus Environment

6

Page 7 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

previous reports (Scheme 1). The products includes arabinose, erythrose, glyceraldehyde, formic acid and hydrogen.35, 36

Scheme 1. Reaction equation for photocatalytic decomposition of glucose by Cu2O@N-CNTs under green light.

In order to further clarify the motors’ propulsion mechanism, a series of controlled experiments on samples including plain N-CNTs particles, plain Cu2O microspheres, and Cu2O@N-CNTs microspheres were systematically performed. Their diameters are all around 1.5 m. Figure 3B shows that, whether in water or in the glucose solution, under the same wavelength of visible light (55300 Lux green light), the plain, non-catalytic N-CNTs particles exhibit similar speeds comparable to their inherent Brownian motion in water without light exposure (speed of 3.54 m/s). These results indicate that such N-CNTs not only lack photocatalytic properties in this condition, but also lack an obvious thermo-responsive behavior under such visible light. It should also be noted that the light-induced heating of the solution also exhibits negligible effects on the Brownian motion of bare N-CNTs particles. In addition, the plain Cu2O particles show enhanced propulsion under 55300 Lux green light, where the speed of the motor in pure water increases from 2.41 m/s to 3.45 m/s due to the photocatalytic properties of Cu2O. In a 30 mM glucose solution under the same light exposure, the speed of the micromotors further increases to 7.15 m/s. These results indicate that Cu2O has higher photocatalytic activity in the presence of glucose compared to in pure water. These control experiments show that the visible light photocatalytic properties

ACS Paragon Plus Environment

7

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 8 of 16

originate from plain Cu2O. Additionally, no obvious thermo-responsive motions of these Cu2O microspheres are observed.

Figure 3. (A) Schematic of propulsion mechanism of light-driven Cu2O@N-CNTs sphere micromotors. (B) Comparison of the velocity of N-CNTs particles, Cu2O spheres and Cu2O@N-CNTs micromotors in different concentrations of glucose solution with or without 55300 Lux green light. The corresponding MSD results are shown in Supporting Information Figure S2.

The Cu2O@N-CNTs micromotors, in a pure water environment without light exposure, also exhibit enhanced Brownian motion with a velocity of 4.57 m/s. Under 55300 Lux green light, the speed of the motors increase to 6.29 m/s and 18.71 m/s in pure water and 30 mM glucose solutions, respectively. Compared with the results of plain Cu2O microspheres, the Cu2O@NCNTs motors show a significant velocity improvement under visible light exposure, especially in the glucose solutions. Therefore, the dramatically increased propulsion of such Cu2O@N-CNTs micromotors in glucose solutions clearly demonstrates that the doped N-CNTs greatly enhance the photocatalytic activity of Cu2O. These results further confirm that the propulsion of the Cu2O@NCNTs micromotors is primarily due to light induced self-diffusiophoresis. In general, diffusiophoresis includes osmophoresis and chemophoresis, which corresponds to nonelectrolyte and electrolyte gradients, respectively. In this system, as discussed previously, the products contain not only neutral molecules (C5H10O5, C4H8O4, C3H6O3, HCOOH, H2) but also cationic and anionic species (HCOO-, H+) produced by the ionization of formic acid. Osmophoresis drives fluid flow to the side of the motor with lower species concentration, which effectively moves the motors away from the light source. Conversely, chemophoretic movement is directed toward higher electrolyte concentrations, which means the motors move towards the light source.20 Therefore, there are two opposing possible diffusion mechanisms in this system. In

ACS Paragon Plus Environment

8

Page 9 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

order to further confirm which is dominating, we have tested the motors under two green lights (X, Y). The lights are parallel with the substrate from two directions. It is obvious from Figures 4A and 4B, the motors exhibit apparent negative phototaxis, and their average speeds here are 11.94 m/s. This result solidly confirms that the propulsion mechanism is dominated by the osmophoretic propulsion. Owing to their excellent negative phototactic behavior, the visible lightdriven motors exhibit efficient direction control by light regulation. As shown in Figure 4B, the motors are moving towards to the upper right with the light X on and light Y off, and are immediately redirected to the upper left with the light X off and light Y on. Such wireless, repeatable, and efficient direction control of these motors is critical to applications in targeted motor transport.

Figure 4. (A) Schematic of Cu2O@N-CNTs micromotors horizontal motion under two green light which are parallel with the substrate from two directions (X, Y). (B) Tracklines of the motors (taken from Video S3). Scale bar: 10 μm. (C) Schematic of the vertical motion of a Cu2O@N-CNTs micromotor under blue light (Z) vertical to the substrate. (D) The time lapse images of the vertical motion of Cu2O@N-CNTs micromotors under blue light (taken from Video S4). Scale bar: 10 μm. (E) Measured velocity of light-induced 3 cyclic on/off motion of Cu2O@N-CNTs micromotors. (F) The corresponding trajectory of a Cu2O@N-CNTs micromotor (taken from Video S5). Scale bar: 10 μm.

In addition to horizontal motion as typically demonstrated with conventional micro/nanomotors, such visible light driven micromotors can also exhibit vertical motion under high energy visible light Z from below. As Figure 4C illustrates, initially the bottom layer of motors are in focus, but when the light Z is turned on, the motors are propelled vertically out of

ACS Paragon Plus Environment

9

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 10 of 16

focus and the camera must be refocused in the upper layer of the test solution. The time-lapse images of the vertical motion are shown in Figure 4D. It can be explained in detail by the previously reported photogravitactic mechanism.37 Briefly, when the light energy is above a sizedependent threshold value,37 it can be used to propel the motors in a vertical direction. The motors are lifted-off from the substrate and swim upward and away from the light source. In contrast, when the light intensity is less than the threshold value, the motors only show horizontal motion as shown in Figure 1, even though the light is still from the bottom and perpendicular to the substrate. As a result, the vertically upward motion of Cu2O@N-CNTs micromotors caused by high energy light from the bottom further confirms the osmophoresis propulsion mechanism. Such attractive micromotors have precise light-controllable three dimensional motion, which holds great potential in various practical applications, especially in cargo targeted delivery. Furthermore, the as-developed visible light-driven Cu2O@N-CNTs micromotors have unique advantages of highly repeatable simple motion control, especially when compared with conventional glucose oxidase-based micromotors (which also consume glucose fuel). As Figures 4E and 4F illustrates, the repeated on/off cycling of visible light illumination induces the activation and inactivation of the movement of micromotors reflecting the fast response rate of the micromotors upon the visible light irradiation. Strong propulsion of motors is generated by the green light exposure, but the motors stop moving immediately when the light is off. This “stop/go” propulsion behavior indicates that high reversibility and controllable micromotor motion can be simply achieved by switching the visible light irradiation on or off (as shown in Supporting Information Video S5). Finally, the speed of such attractive Cu2O@N-CNTs based micromotors can be precisely controlled by multiple methods: adjusting N-CNTs contents, glucose concentrations or light intensities. It is clear from Figure 5A that under a certain condition (55300 Lux green light, 10 mM glucose solution), when the content of N-CNTs is 1.35%, the speed can reach up to the maximum speed of 11.81 m/s, which is double that of a pure Cu2O micromotor. This result can be attributed to the excellent conductivity of N-CNTs. Interestingly, when the content of N-CNTs is greater than 1.35%, the speed begins to decrease. A possible reason is that the excess N-CNTs on the surface hinders the contact of the Cu2O with the green light and suppresses the photocatalytic activity. The N-CNTs content of such motors is measured by thermogravimetric analysis (the method of calculation is described in detail in Supporting Information).

ACS Paragon Plus Environment

10

Page 11 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

Figure 5. (A) The measured speed of micromotors with different N-CNTs content. (B) is the trajectories (taken from Video S6) over 3 seconds of micromotors with different N-CNTs content (0%, 0.91%, 1.35%, 1.72% and 2.35%) in 10 mM glucose solution under visible green illumination (55300 Lux). Scale bar: 10 μm. (C) The velocity of Cu2O@N-CNTs micromotors (1.35% N-CNTs) in different glucose solutions under 55300 Lux visible light, and (D) is the corresponding trajectories over 3 seconds of micromotors (taken from Video S7). Scale bar: 10 μm. (E) The velocity of Cu2O@N-CNTs composite particles (1.35% N-CNTs) with different visible green illumination in 10 mM glucose solution, and (F) is the corresponding trajectories over 3 seconds of samples (taken from Video S8). Scale bar: 10 μm. The corresponding MSD results of Figure A, C, E are shown in Supporting Information Figure S2.

The motor speed control can also be simply realized by adjusting glucose concentration (below 30 Mm). Under 55300 Lux visible light, the motors (1.35% N-CNTs) have weak propulsion in pure water (around 6.29 m/s). When the glucose concentration increases from 5 mM to 10 mM, the speed of micromotors increases from 7.60 m/s to 11.81 m/s. In presence of 30 mM glucose, the motor reaches the absolute highest velocity of 18.71 m/s which is 12 times higher than that of our previously reported water-fueled micromotors also under visible light with similar intensity.38 In addition, such speeds are comparable to the common Pt-based chemically propelled micromotors, which require high levels of H2O2 fuel. Trajectories (Figures 5D) over 3 seconds of samples in 0, 5, 10, 30 mM glucose solutions under 55300 Lux green light further confirm that the motor speed increases with increased glucose concentration.

ACS Paragon Plus Environment

11

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 12 of 16

The speed regulation of Cu2O@N-CNTs micromotors by adjusting the light intensities (I) in a certain concentration (10 mM) glucose solution has been clearly illustrated by Figure 5E. The motor average speed is only 4.56 m/s when the green light is turned off, corresponding to Brownian motion under the ambient light (100 Lux). When the green light intensity is increased to 55300 Lux, the motor speed rapidly increases to 11.81 m/s, which is 2.6 times higher compared with that of the motors without green light illumination. The relationship between incident light (I) and the flux (φ) is described in equation (1): ℎ𝑐

 =φ 𝜆

(1)

Here, I,φ, h, c, and represent the light intensity, the number of incident photons per second per unit area, the Planck's constant (6.626×10-34 J•s), speed of light (3×108 m/s), and the wavelength of green light (510~560nm), respectively. As a result, the fluxφ of the photon of wavelength λ increases as the intensity I on the micromotor increases, thus the number of photogenerated holes and electrons in the Cu2O increases, resulting in stronger photocatalytic propulsion. CONCLUSIONS In summary, we have successfully fabricated Cu2O@N-CNTs based micromotors which can be efficiently propelled by fully green energy sources: renewable visible light and the biofuel glucose. The propulsion mechanism of such micromotors is self-diffusiophoresis, which has been experimentally confirmed. Based on the mechanism, we have demonstrated that a triaxial light source is capable of achieving three dimensional motion control with excellent on/off characteristics. In addition, the attractive propulsion is comparable to that of Pt-based peroxidefueled catalytic micromotors, and can be readily modulated by various approaches: adjusting the N-CNTs contents within the micromotors, the glucose concentrations or light intensities. This is the first demonstration of using photocatalysis to convert the chemical energy of glucose to mechanical energy of a micromotor. Through this method, the upper limit of glucose-fueled micromotors’ propulsion has been greatly improved. Such photocatalytic methods are extremely efficient, stable and easy operated compared to previously reported enzymatic methods. The attractive photocatalytic glucose-fueled micromotors with highly efficient, fully biocompatible and flexibly light-regulated characteristics promise a great potential in a wide range of fields. Since visible light can't penetrate body tissues, there still be a challenge to apply this system in bio-

ACS Paragon Plus Environment

12

Page 13 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

applications. As a result, it is desirable to explore the next generation glucose-fueled micromotors which can be powered by infrared radiation (IR). The following efforts will be devoted to improving the photocatalytic performance of IR photocatalysts and optimizing the structures of motors in order to develop highly efficient IR activated glucose-fueled micro/nanomotors for biological or biomedical applications in future.

ASSOCIATED CONTENT Supporting Information. XPS, TG data of as-synthesized Cu2O@N-CNTs micromotors and corresponding videos. AUTHOR INFORMATION Corresponding Author *E-mail: [email protected] (Renfeng Dong) *E-mail: [email protected] (Yuepeng Cai) Financial Interest Statements The authors declare no competing financial interest. Author Contributions 

Qinglong Wang and Renfeng Dong contributed equally.

ACKNOWLEDGMENT The authors are grateful for the Natural Science Foundation of China (21805096), Natural Science Foundation of Guangdong Province (2018A030313358, 2017A030310432), the National Natural Science Foundation of China (21674039, 21471061, 21671071), Applied Science and Technology Planning Project of Guangdong Province (2015B010135009, 2017B090917002). Innovation team project of Guangdong Ordinary University (2015KCXTD005), the great scientific research project of Guangdong Ordinary University (2016KZDXM023).

ACS Paragon Plus Environment

13

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 14 of 16

REFERENCES 1. 2. 3. 4.

5. 6. 7. 8.

9. 10. 11. 12. 13. 14. 15. 16. 17.

Xu, T.; Soto, F.; Gao, W.; Garcia-Gradilla, V.; Li, J.; Zhang, X.; Wang, J., UltrasoundModulated Bubble Propulsion of Chemically Powered Microengines. J. Am. Chem. Soc. 2014, 136 (24), 8552-8555. Xu, T.; Soto, F.; Gao, W.; Dong, R.; Garcia-Gradilla, V.; Magaña, E.; Zhang, X.; Wang, J., Reversible Swarming and Separation of Self-Propelled Chemically Powered Nanomotors under Acoustic Fields. J. Am. Chem. Soc. 2015, 137 (6), 2163-2166. Peyer, K. E.; Tottori, S.; Qiu, F.; Zhang, L.; Nelson, B. J., Magnetic Helical Micromachines. Chem. Eur. J. 2013, 19 (1), 28-38. Jinxing, L.; Pavimol, A.; Wenjuan, L.; Berta, E.-F. d. Á.; Xiaocong, C.; Elodie, S.; Yuyan, L.; Siyu, Z.; Yue, Z.; Chuanrui, C.; Weiwei, G.; Liangfang, Z.; Joseph, W., Biomimetic Platelet-Camouflaged Nanorobots for Binding and Isolation of Biological Threats. Adv. Mater. 2018, 30 (2), 1704800. Calvo-Marzal, P.; Sattayasamitsathit, S.; Balasubramanian, S.; Windmiller, J. R.; Dao, C.; Wang, J., Propulsion of Nanowire Diodes. Chem. Commun. 2010, 46 (10), 1623-1624. Loget, G.; Kuhn, A., Electric Field-Induced Chemical Locomotion of Conducting Objects. Nat. Commun. 2011, 2, 535. Xu, T.; Xu, L.-P.; Zhang, X., Ultrasound Propulsion of Micro-/Nanomotors. Appl. Mater. Today 2017, 9, 493-503. Esteban-Fernández de Ávila, B.; Angsantikul, P.; Ramírez-Herrera, D. E.; Soto, F.; Teymourian, H.; Dehaini, D.; Chen, Y.; Zhang, L.; Wang, J., Hybrid Biomembrane– Functionalized Nanorobots for Concurrent Removal of Pathogenic Bacteria and Toxins. Science Robotics 2018, 3 (18). Xu, L.; Mou, F.; Gong, H.; Luo, M.; Guan, J., Light-Driven Micro/Nanomotors: From Fundamentals to Applications. Chem. Soc. Rev. 2017, 46 (22), 6905-6926. Wu, Z.; Gao, C.; Frueh, J.; Sun, J.; He, Q., Remote-Controllable Explosive Polymer Multilayer Tubes for Rapid Cancer Cell Killing. Macromol. Rapid Commun. 2015, 36 (15), 1444-1449. Soler, L.; Sánchez, S., Catalytic Nanomotors for Environmental Monitoring and Water Remediation. Nanoscale 2014, 6 (13), 7175-7182. Jurado-Sánchez, B.; Wang, J., Micromotors for Environmental Applications: A Review. Environ. Sci-Nano. 2018, 5 (7), 1530-1544. Kim, K.; Guo, J.; Liang, Z.; Fan, D., Artificial Micro/Nanomachines for Bioapplications: Biochemical Delivery and Diagnostic Sensing. Adv. Funct. Mater. 2018, 28 (25), 1705867. Luo, M.; Feng, Y.; Wang, T.; Guan, J., Micro-/Nanorobots at Work in Active Drug Delivery. Adv. Funct. Mater. 2018, 28 (25), 1706100. Paxton, W. F.; Kistler, K. C.; Olmeda, C. C.; Sen, A.; St. Angelo, S. K.; Cao, Y.; Mallouk, T. E.; Lammert, P. E.; Crespi, V. H., Catalytic Nanomotors:  Autonomous Movement of Striped Nanorods. J. Am. Chem. Soc. 2004, 126 (41), 13424-13431. Yoshizumi, Y.; Date, Y.; Ohkubo, K.; Yokokawa, M.; Suzuki, H. In Bimetallic micromotor autonomously movable in biofuels, 2013 IEEE 26th International Conference on Micro Electro Mechanical Systems (MEMS), 20-24 Jan. 2013; 2013; pp 540-543. Xu, B.; Zhang, B.; Wang, L.; Huang, G.; Mei, Y., Tubular Micro/Nanomachines: From the Basics to Recent Advances. Adv. Funct. Mater. 2018, 28 (25), 1705872.

ACS Paragon Plus Environment

14

Page 15 of 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

18. Zhang, Y.; Zhu, H.; Qiu, W.; Zhou, Y.; Huang, G.; Mei, Y.; Solovev, A. A., Carbon Dioxide Bubble-Propelled Microengines in Carbonated Water and Beverages. Chem. Commun. 2018, 54 (45), 5692-5695. 19. Jurado-Sánchez, B.; Pacheco, M.; Maria-Hormigos, R.; Escarpa, A., Perspectives on Janus Micromotors: Materials and Applications. Appl. Mater. Today 2017, 9, 407-418. 20. Gao, W.; Pei, A.; Dong, R.; Wang, J., Catalytic Iridium-Based Janus Micromotors Powered by Ultralow Levels of Chemical Fuels. J. Am. Chem. Soc. 2014, 136 (6), 2276-2279. 21. Peng, F.; Men, Y.; Tu, Y.; Chen, Y.; Wilson, D. A., Nanomotor-Based Strategy for Enhanced Penetration across Vasculature Model. Adv. Funct. Mater. 2018, 28 (25), 1706117. 22. Peng, F.; Tu, Y.; Men, Y.; Hest, J. C. M. v.; Wilson, D. A., Supramolecular Adaptive Nanomotors with Magnetotaxis Behavior. Adv. Mater. 2017, 29 (6), 1604996. 23. Schattling, P. S.; Ramos-Docampo, M. A.; Salgueiriño, V.; Städler, B., Double-Fueled Janus Swimmers with Magnetotactic Behavior. ACS Nano 2017, 11 (4), 3973-3983. 24. Sengupta, S.; Patra, D.; Ortiz-Rivera, I.; Agrawal, A.; Shklyaev, S.; Dey, K. K.; CórdovaFigueroa, U.; Mallouk, T. E.; Sen, A., Self-Powered Enzyme Micropumps. Nat. Chem. 2014, 6, 415-422. 25. He, J.; Jiang, Y.; Peng, J.; Li, C.; Yan, B.; Wang, X., Fast Synthesis of Hierarchical Cuprous Oxide for Nonenzymatic Glucose Biosensors with Enhanced Sensitivity. J. Mater. Sci. 2016, 51 (21), 9696-9704. 26. Fu, X.; Long, J.; Wang, X.; Leung, D. Y. C.; Ding, Z.; Wu, L.; Zhang, Z.; Li, Z.; Fu, X., Photocatalytic Reforming of Biomass: A Systematic Study of Hydrogen Evolution from Glucose Solution. Int. J. Hydrogen Energ. 2008, 33 (22), 6484-6491. 27. Nakamura, H.; Tanaka, M.; Shinohara, S.; Gotoh, M.; Karube, I., Development of a SelfSterilizing Lancet Coated with A Titanium Dioxide Photocatalytic Nano-Layer for SelfMonitoring of Blood Glucose. Biosens. Bioelectron. 2007, 22 (9), 1920-1925. 28. Li, Y.; Zhong, Y.; Zhang, Y.; Weng, W.; Li, S., Carbon Quantum Dots/Octahedral Cu2O Nanocomposites for Non-Enzymatic Glucose and Hydrogen Peroxide Amperometric Sensor. Sensor. Actuat. B-Chem 2015, 206, 735-743. 29. Lee, W. J.; Maiti, U. N.; Lee, J. M.; Lim, J.; Han, T. H.; Kim, S. O., Nitrogen-Doped Carbon Nanotubes and Graphene Composite Structures for Energy and Catalytic Applications. Chem. Commun. 2014, 50 (52), 6818-6830. 30. Zeng, B.; Chen, X.; Ning, X.; Chen, C.; Deng, W.; Huang, Q.; Zhong, W., ElectrostaticAssembly Three-Dimensional CNTs/rGO Implanted Cu2O Composite Spheres and Its Photocatalytic Properties. Appl. Surf. Sci. 2013, 276, 482-486. 31. Wang, J.; Xiong, Z.; Zheng, J.; Zhan, X.; Tang, J., Light-Driven Micro/Nanomotor for Promising Biomedical Tools: Principle, Challenge, and Prospect. Acc. Chem. Res. 2018,51 (9), 1957–1965. 32. Zhang, Q.; Dong, R.; Chang, X.; Ren, B.; Tong, Z., Spiropyran-Decorated SiO2–Pt Janus Micromotor: Preparation and Light-Induced Dynamic Self-Assembly and Disassembly. ACS Appl. Mater. Inter. 2015, 7 (44), 24585-24591. 33. Yu, H.; Peng, F.; Tan, J.; Hu, X.; Wang, H.; Yang, J.; Zheng, W., Selective Catalysis of the Aerobic Oxidation of Cyclohexane in the Liquid Phase by Carbon Nanotubes. Angew. Chem. 2011, 123 (17), 4064-4068. 34. Cao, Y.; Yu, H.; Tan, J.; Peng, F.; Wang, H.; Li, J.; Zheng, W.; Wong, N.-B., Nitrogen-, Phosphorous- and Boron-Doped Carbon Nanotubes as Catalysts for the Aerobic Oxidation of Cyclohexane. Carbon 2013, 57, 433-442.

ACS Paragon Plus Environment

15

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 16 of 16

35. Vià, L. D.; Recchi, C.; Gonzalez-Yañez, E. O.; Davies, T. E.; Lopez-Sanchez, J. A., Visible Light Selective Photocatalytic Conversion of Glucose by TiO2. Appl. Catal. B-Environ. 2017, 202, 281-288. 36. Chong, R.; Li, J.; Ma, Y.; Zhang, B.; Han, H.; Li, C., Selective Conversion of Aqueous Glucose to Value-Added Sugar Aldose on TiO2-Based Photocatalysts. J. Catal. 2014, 314, 101-108. 37. Singh, D. P.; Uspal, W. E.; Popescu, M. N.; Wilson, L. G.; Fischer, P., Photogravitactic Microswimmers. Adv. Funct. Mater. 2018, 28 (25), 1706660. 38. Dong, R.; Hu, Y.; Wu, Y.; Gao, W.; Ren, B.; Wang, Q.; Cai, Y., Visible-Light-Driven BiOIBased Janus Micromotor in Pure Water. J. Am. Chem. Soc. 2017, 139 (5), 1722-1725.

TOC Graphic

ACS Paragon Plus Environment

16