IRG 2 - Powered Motion at the Nanoscale

DDNA polymerase is one of several enzymes that have no known motor function in biology, but has nevertheless been shown by IRG researchers to act as single-molecule motor and pump. Enzyme motors also exhibit unexpected
chemotactic behavior, which can be harnessed for directional motion of enzymes and enzyme-attached microparticles.

Leader:  Ayusman Sen

Description

IRG2 makes, models, and studies autonomous motors and pumps that convert the free energy of local chemical, optical, thermal, and acoustic fields to motion. In addition to providing information about the mechanisms of motility, the study of synthetic motors helps address fundamental questions about emergent collective behavior at low Reynolds number and on length scales from sub-nanometers to many micrometers. Much of our understanding of active matter derives from continuum theories coupled to observations of complex biological swimmers or externally driven colloidal particles. The observation in abiotic systems of many behaviors previously associated with purely biological processes suggest intriguing questions as to the underlying principles that govern both. The IRG2 team pursues a bottom-up approach to understanding motility, sensing and emergent collective behavior in autonomously driven synthetic systems by combining theory and numerical modeling with the synthesis and experimental study of new classes of motors.

Important findings in IRG2 include the discovery of synthetic autonomous nanomotors and micropumps driven by catalysis and light, elucidation of their self-electrophoretic and diffusiophoretic propulsion mechanisms, discovery of complex swarming, predator-prey, and spatio-temporal oscillatory behavior in colloidal motor assemblies, engineering of chemotaxis, steering, and cargo delivery in motor systems, demonstration of catalytically powered motion at the nm scale of individual catalyst molecules, including (non-motor) enzyme molecules, characterization of momentum transfer by active swimmers at length scales from colloidal to molecular, and discovery of novel acoustic motor propulsion mechanisms that are tolerant of electrolyte solutions and gel media, including the interior of living cells.

Recent Accomplishments:

  • Showed that catalysts, ranging from molecules to microparticles, undergo directional chemotactic movement in the presence of substrate gradients.8,16,20,56,65
  • Observed emergent swarming and predator-prey behavior due to chemotaxis for particles and enzyme molecules that produce self-generated chemical gradients: Achieved control over formation of zones of attraction and exclusion, as well as spatiotemporal reversibility.17,31,55,65
  • Observed enhanced diffusive motion of individual molecular catalysts and single enzyme molecules in the presence of their specific substrates.8,16,22,28,56,57,62
  • Demonstrated motors can be powered by ultrasound and exhibit speeds of up to hundreds of microns per second. Emergent collective behavior, including the reversible assembly of multimetallic rods into geometrically regular multimers have been observed.4,13,14,17,36,39,46,53,59
  • Showed that catalytic Janus particles in proximity to a surface undergo constrained in-plane swimming along the wall. The ability to steer Janus motor particles unidirectionally along complicated trajectories by simply following an edge or groove opens the door for many transport and separation tasks.27,59
  • Determined that surface-anchored enzymes pump fluid in the presence of their respective substrates.35,37,42,54,56
  • Designed self-powered devices for on-demand controlled drug and antidote delivery and for sensing toxic substances in the environment that exploits pumping fluid via enzymes.20,35
  • Revealed that trisegmented Au-Ru-Au and Ru-Au-Ru rods trigger electrokinetic fluid pumping along their axis as “pullers” and “pushers”, respectively: Catalytically generated hydrodynamic and electrostatic forces both contribute to pairwise and collective particle assembly.34
  • Demonstrated that enzymes tethered to microparticles impart directional motility to the particles.26
  • Observed chemically-driven convective flows leading to transport in and out of dead-end pores that occurs by the phenomenon of “transient diffusioosmosis”. This illustrates that chemical energy in the form of a transient salt gradient can be transduced into mechanical motion, with the pore wall acting as the pump. This phenomena may underlie observed transport in many geological and biological systems involving tight or dead-end micro and nano-channels.6
  • Publications

65.        Zhao, X.; Palacci, H.; Yadav, V.; Spiering, M. M.; Gilson, M. K.; Butler, P. J.; Hess, H.; Benkovic, S. J.; Sen, A. Substrate-Driven Chemotactic Assembly in an Enzyme Cascade. Nature Chem 2017, 10 (3), 311–317. DOI: 10.1038/nchem.2905

64.        Agudo-Canalejo, J.; Golestanian, R. Pattern Formation by Curvature-Inducing Proteins on Spherical Membranes. New J. Phys. 2017, 19 (12), 125013. DOI: 10.1088/1367-2630/aa983c

63.        Guha, R.; Mohajerani, F.; Mukhopadhyay, A.; Collins, M. D.; Sen, A.; Velegol, D. Modulation of Spatiotemporal Particle Patterning in Evaporating Droplets: Applications to Diagnostics and Materials Science. ACS Appl. Mater. Interfaces 2017, 9 (49), 43352–43362. DOI: 10.1021/acsami.7b13675

62.        Illien, P.; Adeleke-Larodo, T.; Golestanian, R. Diffusion of an Enzyme: The Role of Fluctuation-Induced Hydrodynamic Coupling. EPL 2017, 119 (4), 40002. DOI: 10.1209/0295-5075/119/40002

61.        Guha, R.; Mohajerani, F.; Collins, M.; Ghosh, S.; Sen, A.; Velegol, D. Chemotaxis of Molecular Dyes in Polymer Gradients in Solution. J. Am. Chem. Soc. 2017, 139 (44), 15588–15591. DOI: 10.1021/jacs.7b08783

60.        Byun, Y.-M.; Lammert, P. E.; Hong, Y.; Sen, A.; Crespi, V. H. Distinguishing Advective and Powered Motion in Self-Propelled Colloids. J. Phys.: Condens. Matter 2017, 29 (44), 445101. DOI: 10.1088/1361-648X/aa88f1

59.        Ren, L.; Zhou, D.; Mao, Z.; Xu, P.; Huang, T. J.; Mallouk, T. E. Rheotaxis of Bimetallic Micromotors Driven by Chemical–Acoustic Hybrid Power. ACS Nano 2017, 11 (10), 10591–10598. DOI: 10.1021/acsnano.7b06107

58.        Zhao, X.; Dey, K. K.; Jeganathan, S.; Butler, P. J.; Córdova-Figueroa, U. M.; Sen, A. Enhanced Diffusion of Passive Tracers in Active Enzyme Solutions. Nano Lett. 2017, 17 (8), 4807–4812. DOI: 10.1021/acs.nanolett.7b01618

57.        Illien, P.; Zhao, X.; Dey, K. K.; Butler, P. J.; Sen, A.; Golestanian, R. Exothermicity Is Not a Necessary Condition for Enhanced Diffusion of Enzymes. Nano Lett. 2017, 17 (7), 4415–4420. DOI: 10.1021/acs.nanolett.7b01502

56.        Dey, K. K.; Sen, A. Chemically Propelled Molecules and Machines. J. Am. Chem. Soc. 2017, 139 (23), 7666–7676. DOI: 10.1021/jacs.7b02347

55.        Altemose, A.; Sánchez-Farrán, M. A.; Duan, W.; Schulz, S.; Borhan, A.; Crespi, V. H.; Sen, A. Chemically Controlled Spatiotemporal Oscillations of Colloidal Assemblies. Angew. Chem. Int. Ed. 2017, 56 (27), 7817–7821. DOI: 10.1002/anie.201703239

54.        Das, S.; Shklyaev, O. E.; Altemose, A.; Shum, H.; Ortiz-Rivera, I.; Valdez, L.; Mallouk, T. E.; Balazs, A. C.; Sen, A. Harnessing Catalytic Pumps for Directional Delivery of Microparticles in Microchambers. Nat Comms 2017, 8, 14384. DOI: 10.1038/ncomms14384

53.        Kaynak, M.; Ozcelik, A.; Nourhani, A.; Lammert, P. E.; Crespi, V. H.; Huang, T. J. Acoustic Actuation of Bioinspired Microswimmers. Lab on a Chip 2017, 17, 395–400. DOI: 10.1039/C6LC01272H

52.        Illien, P.; Golestanian, R.; Sen, A. “Fuelled” Motion: Phoretic Motility and Collective Behaviour of Active Colloids. Chem. Soc. Rev. 2017, 46 (18), 5508–5518. DOI: 10.1039/C7CS00087A

51.        Zhou, D.; Li, Y. C.; Xu, P.; McCool, N. S.; Li, L.; Wang, W.; Mallouk, T. E. Visible-Light Controlled Catalytic Cu2O–Au Micromotors. Nanoscale 2017, 9 (1), 75–78. DOI: 10.1039/C6NR08088J

50.        Zhou, D.; Ren, L.; Li, Y. C.; Xu, P.; Gao, Y.; Zhang, G.; Wang, W.; Mallouk, T. E.; Li, L. Visible Light-Driven, Magnetically Steerable Gold/Iron Oxide Nanomotors. Chem. Commun. 2017, 53 (83), 11465–11468. DOI: 10.1039/C7CC06327J

49.        Zhou, D.; Li, Y. C.; Xu, P.; Ren, L.; Zhang, G.; Mallouk, T. E.; Li, L. Visible-Light Driven Si–Au Micromotors in Water and Organic Solvents. Nanoscale 2017, 9 (32), 11434–11438. DOI: 10.1039/C7NR04161F

48.        Garg, A.; Cartier, C. A.; Bishop, K. J. M.; Velegol, D. Particle Zeta Potentials Remain Finite in Saturated Salt Solutions. Langmuir 2016, 32 (45), 11837–11844. DOI: 10.1021/acs.langmuir.6b02824

47.        Lata, J. P.; Guo, F.; Guo, J.; Huang, P.-H.; Yang, J.; Huang, T. J. Surface Acoustic Waves Grant Superior Spatial Control of Cells Embedded in Hydrogel Fibers. Adv. Mater. 2016, 28 (39), 8632–8638. DOI: 10.1002/adma.201602947

46.        Kaynak, M.; Ozcelik, A.; Nama, N.; Nourhani, A.; Lammert, P. E.; Crespi, V. H.; Huang, T. J. Acoustofluidic Actuation of in Situ Fabricated Microrotors. Lab on a Chip 2016, 16, 3532–3537. DOI: 10.1039/C6LC00443A

45.        Ozcelik, A.; Nama, N.; Huang, P.-H.; Kaynak, M.; McReynolds, M. R.; Hanna-Rose, W.; Huang, T. J. Acoustofluidic Rotational Manipulation of Cells and Organisms Using Oscillating Solid Structures. Small 2016, 12 (37), 5120–5125. DOI: 10.1002/smll.201601760

44.        Lammert, P. E.; Crespi, V. H.; Nourhani, A. Bypassing Slip Velocity: Rotational and Translational Velocities of Autophoretic Colloids in Terms of Surface Flux. J. Fluid Mech. 2016, 802, 294–304. DOI: 10.1017/jfm.2016.460

43.        Wong, F.; Sen, A. Progress Toward Light-Harvesting Self-Electrophoretic Motors: Highly Efficient Bimetallic Nanomotors and Micropumps in Halogen Media. ACS Nano 2016, 10 (7), 7172–7179. DOI: 10.1021/acsnano.6b03474

42.        Wong, F.; Dey, K. K.; Sen, A. Synthetic Micro/Nanomotors and Pumps: Fabrication and Applications. Annu. Rev. Mater. Res. 2016, 46 (1), 407–432. DOI: 10.1146/annurev-matsci-070115-032047

41.        Tang, S.-Y.; Ayan, B.; Nama, N.; Bian, Y.; Lata, J. P.; Guo, X.; Huang, T. J. On-Chip Production of Size-Controllable Liquid Metal Microdroplets Using Acoustic Waves. Small 2016, 12 (28), 3861–3869. DOI: 10.1002/smll.201600737

40.        Kar, A.; McEldrew, M.; Stout, R. F.; Mays, B. E.; Khair, A.; Velegol, D.; Gorski, C. A. Self-Generated Electrokinetic Fluid Flows During Pseudomorphic Mineral Replacement Reactions. Langmuir 2016, 32 (21), 5233–5240. DOI: 10.1021/acs.langmuir.6b00462

39.        Ahmed, S.; Wang, W.; Bai, L.; Gentekos, D. T.; Hoyos, M.; Mallouk, T. E. Density and Shape Effects in the Acoustic Propulsion of Bimetallic Nanorod Motors. ACS Nano 2016, 10 (4), 4763–4769. DOI: 10.1021/acsnano.6b01344

38.        Ahmed, D.; Ozcelik, A.; Bojanala, N.; Nama, N.; Upadhyay, A.; Chen, Y.; Hanna-Rose, W.; Huang, T. J. Rotational Manipulation of Single Cells and Organisms Using Acoustic Waves. Nat Comms 2016, 7, 11085. DOI: 10.1038/ncomms11085

37.        Ortiz-Rivera, I.; Shum, H.; Agrawal, A.; Sen, A.; Balazs, A. C. Convective Flow Reversal in Self-Powered Enzyme Micropumps. Proc. Natl. Acad. Sci. USA 2016, 113 (10), 2585–2590. DOI: 10.1073/pnas.1517908113

36.        Nama, N.; Huang, P.-H.; Huang, T. J.; Costanzo, F. Investigation of Micromixing by Acoustically Oscillated Sharp-Edges. Biomicrofluidics 2016, 10 (2), 024124. DOI: 10.1063/1.4946875

35.        Ortiz-Rivera, I.; Courtney, T. M.; Sen, A. Enzyme Micropump-Based Inhibitor Assays. Adv. Funct. Mater. 2016, 26 (13), 2135–2142. DOI: 10.1002/adfm.201504619

34.        Jewell, E. L.; Wang, W.; Mallouk, T. E. Catalytically Driven Assembly of Trisegmented Metallic Nanorods and Polystyrene Tracer Particles. Soft Matter 2016, 12, 2501–2504. DOI: 10.1039/C5SM03066H

33.        Kar, A.; Chiang, T.-Y.; Rivera, I. O.; Sen, A.; Velegol, D. Correction to Enhanced Transport Into and Out of Dead-End Pores. ACS Nano 2016, 10 (3), 3871–3871. DOI: 10.1021/acsnano.6b00965

32.        Guo, F.; Mao, Z.; Chen, Y.; Xie, Z.; Lata, J. P.; Li, P.; Ren, L.; Liu, J.; Yang, J.; Dao, M.; Suresh, S.; Huang, T. J. Three-Dimensional Manipulation of Single Cells Using Surface Acoustic Waves. Proc. Natl. Acad. Sci. USA 2016, 113 (6), 1522–1527. DOI: 10.1073/pnas.1524813113

31.        Dey, K. K.; Wong, F.; Altemose, A.; Sen, A. Catalytic Motors—Quo Vadimus? Curr. Opin. Colloid Interface Sci. 2016, 21, 4–13. DOI: 10.1016/j.cocis.2015.12.001

30.        Mao, Z.; Xie, Y.; Guo, F.; Ren, L.; Huang, P.-H.; Chen, Y.; Rufo, J.; Costanzo, F.; Huang, T. J. Experimental and Numerical Studies on Standing Surface Acoustic Wave Microfluidics. Lab on a Chip 2016, 16, 515–524. DOI: 10.1039/C5LC00707K

29.        Xie, Y.; Nama, N.; Li, P.; Mao, Z.; Huang, P.-H.; Zhao, C.; Costanzo, F.; Huang, T. J. Probing Cell Deformability via Acoustically Actuated Bubbles. Small 2015, 12 (7), 902–910. DOI: 10.1002/smll.201502220

28.        Dey, K. K.; Pong, F. Y.; Breffke, J.; Pavlick, R.; Hatzakis, E.; Pacheco, C.; Sen, A. Dynamic Coupling at the Ångström Scale. Angew. Chem. Int. Ed. 2015, 55 (3), 1113–1117. DOI: 10.1002/anie.201509237

27.        Das, S.; Garg, A.; Campbell, A. I.; Howse, J.; Sen, A.; Velegol, D.; Golestanian, R.; Ebbens, S. J. Boundaries Can Steer Active Janus Spheres. Nat Comms 2015, 6 (1), 8999. DOI: 10.1038/ncomms9999

26.        Dey, K. K.; Zhao, X.; Tansi, B. M.; Méndez-Ortiz, W. J.; Córdova-Figueroa, U. M.; Golestanian, R.; Sen, A. Micromotors Powered by Enzyme Catalysis. Nano Lett. 2015, 15 (12), 8311–8315. DOI: 10.1021/acs.nanolett.5b03935

25.        Nourhani, A.; Crespi, V. H.; Lammert, P. E.; Borhan, A. Self-Electrophoresis of Spheroidal Electrocatalytic Swimmers. Physics of Fluids 2015, 27 (9), 092002. DOI: 10.1063/1.4929518

 

24.        Ren, L.; Chen, Y.; Li, P.; Mao, Z.; Huang, P.-H.; Rufo, J.; Guo, F.; Wang, L.; McCoy, J. P.; Levine, S. J.; Huang, T. J. A High-Throughput Acoustic Cell Sorter. Lab on a Chip 2015, 15, 3870–3879. DOI: 10.1039/C5LC00706B

23.        Nourhani, A.; Crespi, V. H.; Lammert, P. E. Guiding Chiral Self-Propellers in a Periodic Potential. Phys. Rev. Lett. 2015, 115 (11), 118101. DOI: 10.1103/PhysRevLett.115.118101

22.        Golestanian, R. Enhanced Diffusion of Enzymes That Catalyze Exothermic Reactions. Phys. Rev. Lett. 2015, 115 (10), 108102. DOI: 10.1103/PhysRevLett.115.108102

21.        Ahmed, D.; Peng, X.; Ozcelik, A.; Zheng, Y.; Huang, T. J. Acousto-Plasmofluidics: Acoustic Modulation of Surface Plasmon Resonance in Microfluidic Systems. AIP Advances 2015, 5 (9), 097161. DOI: 10.1063/1.4931641

20.        Duan, W.; Wang, W.; Das, S.; Yadav, V.; Mallouk, T. E.; Sen, A. Synthetic Nano- and Micromachines in Analytical Chemistry: Sensing, Migration, Capture, Delivery, and Separation. Annu. Rev. Anal. Chem. 2015, 8 (1), 311–333. DOI: 10.1146/annurev-anchem-071114-040125

19.        Xie, Y.; Chindam, C.; Nama, N.; Yang, S.; Lu, M.; Zhao, Y.; Mai, J. D.; Costanzo, F.; Huang, T. J. Exploring Bubble Oscillation and Mass Transfer Enhancement in Acoustic-Assisted Liquid-Liquid Extraction with a Microfluidic Device. Sci. Rep. 2015, 5 (1), 12572. DOI: 10.1038/srep12572

18.        Wang, M.; Zhao, C.; Miao, X.; Zhao, Y.; Rufo, J.; Liu, Y. J.; Huang, T. J.; Zheng, Y. Plasmofluidics: Merging Light and Fluids at the Micro-/Nanoscale. Small 2015, 11 (35), 4423–4444. DOI: 10.1002/smll.201500970

17.        Wang, W.; Duan, W.; Ahmed, S.; Sen, A.; Mallouk, T. E. From One to Many: Dynamic Assembly and Collective Behavior of Self-Propelled Colloidal Motors. Acc. Chem. Res. 2015, 48 (7), 1938–1946. DOI: 10.1021/acs.accounts.5b00025

16.        Yadav, V.; Duan, W.; Butler, P. J.; Sen, A. Anatomy of Nanoscale Propulsion. Annu. Rev. Biophys. 2015, 44 (1), 77–100. DOI: 10.1146/annurev-biophys-060414-034216

15.        Nourhani, A.; Crespi, V. H.; Lammert, P. E. Self-Consistent Nonlocal Feedback Theory for Electrocatalytic Swimmers with Heterogeneous Surface Chemical Kinetics. Phys. Rev. E 2015, 91 (6), 062303. DOI: 10.1103/PhysRevE.91.062303

14.        Nama, N.; Barnkob, R.; Mao, Z.; Kähler, C. J.; Costanzo, F.; Huang, T. J. Numerical Study of Acoustophoretic Motion of Particles in a PDMS Microchannel Driven by Surface Acoustic Waves. Lab on a Chip 2015, 15, 2700–2709. DOI: 10.1039/C5LC00231A

13.        Ahmed, D.; Lu, M.; Nourhani, A.; Lammert, P. E.; Stratton, Z.; Muddana, H. S.; Crespi, V. H.; Huang, T. J. Selectively Manipulable Acoustic-Powered Microswimmers. Sci. Rep. 2015, 5 (1), 9744. DOI: 10.1038/srep09744

12.        Yazdi, S.; Ardekani, A. M.; Borhan, A. Swimming Dynamics Near a Wall in a Weakly Elastic Fluid. Journal of Nonlinear Science 2015, 25 (5), 1153–1167. DOI: 10.1007/s00332-015-9253-x

11.        Li, P.; Mao, Z.; Peng, Z.; Zhou, L.; Chen, Y.; Huang, P.-H.; Truica, C. I.; Drabick, J. J.; El-Deiry, W. S.; Dao, M.; Suresh, S.; Huang, T. J. Acoustic Separation of Circulating Tumor Cells. Proc. Natl. Acad. Sci. USA 2015, 112 (16), 4970–4975. DOI:

10.        Guo, F.; Zhou, W.; Li, P.; Mao, Z.; Yennawar, N. H.; French, J. B.; Huang, T. J. Precise Manipulation and Patterning of Protein Crystals for Macromolecular Crystallography Using Surface Acoustic Waves. Small 2015, 11 (23), 2733–2737. DOI: 10.1002/smll.201403262

9.          Mao, Z.; Guo, F.; Xie, Y.; Zhao, Y.; Lapsley, M. I.; Wang, L.; Mai, J. D.; Costanzo, F.; Huang, T. J. Label-Free Measurements of Reaction Kinetics Using a Droplet-Based Optofluidic Device. J Lab Autom. 2015, 20 (1), 17–24. DOI: 10.1177/2211068214549625

8.          Butler, P. J.; Dey, K. K.; Sen, A. Impulsive Enzymes: a New Force in Mechanobiology. Cel. Mol. Bioeng. 2015, 8 (1), 106–118. DOI: 10.1007/s12195-014-0376-1

7.          Guo, F.; Li, P.; French, J. B.; Mao, Z.; Zhao, H.; Li, S.; Nama, N.; Fick, J. R.; Benkovic, S. J.; Huang, T. J. Controlling Cell–Cell Interactions Using Surface Acoustic Waves. Proc. Natl. Acad. Sci. USA 2015, 112 (1), 43–48. DOI: 10.1073/pnas.1422068112

6.          Kar, A.; Chiang, T.-Y.; Ortiz-Rivera, I.; Sen, A.; Velegol, D. Enhanced Transport Into and Out of Dead-End Pores. ACS Nano 2015, 9 (1), 746–753. DOI: 10.1021/nn506216b

5.          Nourhani, A.; Lammert, P. E.; Crespi, V. H.; Borhan, A. A General Flux-Based Analysis for Spherical Electrocatalytic Nanomotors. Physics of Fluids 2015, 27 (1), 012001. DOI: 10.1063/1.4904951

4.          Wang, W.; Duan, W.; Zhang, Z.; Sun, M.; Sen, A.; Mallouk, T. E. A Tale of Two Forces: Simultaneous Chemical and Acoustic Propulsion of Bimetallic Micromotors. Chem. Commun. (Camb.) 2014, 51, 1020–1023. DOI: 10.1039/C4CC09149C

3.          Nourhani, A.; Crespi, V. H.; Lammert, P. E. Gaussian Memory in Kinematic Matrix Theory for Self-Propellers. Phys. Rev. E 2014, 90 (6), 239. DOI: 10.1103/PhysRevE.90.062304

2.          Li, S.; Ding, X.; Mao, Z.; Chen, Y.; Nama, N.; Guo, F.; Li, P.; Wang, L.; Cameron, C. E.; Huang, T. J. Standing Surface Acoustic Wave (SSAW)-Based Cell Washing. Lab on a Chip 2014, 15, 331–338. DOI: 10.1039/C4LC00903G

1.          Nourhani, A.; Lammert, P. E.; Borhan, A.; Crespi, V. H. Kinematic Matrix Theory and Universalities in Self-Propellers and Active Swimmers. Phys. Rev. E 2014, 89 (6), 498. DOI: 10.1103/PhysRevE.89.062304