IRG 2 - Powered Motion at the Nanoscale

DNA polymerase is one of several enzymes that have no known motor function in biology, but have nevertheless been shown by IRG researchers to act as single-molecule motors and pumps. Enzyme motors also exhibit unexpected chemotactic behavior, which can be

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 hundreds of 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 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 two new acoustic motor propulsion mechanisms that are tolerant of electrolyte solutions and gel media, including the interior of living cells.

Recent Accomplishments:

  • Individual molecular catalysts and single enzyme molecules show enhanced diffusive motion in the presence of their specific substrates (J. Am. Chem. Soc., 2010, 2013; Nano Lett., 2014; Phys. Rev. Lett., 2015; Angew. Chem., 2015).
  • The enzymes can be tethered to microparticles to impart directional motility (Nano Lett., 2015).
  • Catalysts, from molecules to microparticles, undergo directional chemotactic movement in the presence of substrate gradients (J. Am. Chem. Soc., 2013; Nano Lett., 2014, 2015).
  • Surface-anchored enzymes pump fluid in presence of their respective substrates (Nature Chem., 2014; Proc. Nat. Acad. Sci., 2016).
  • Fluid pumping by enzymes can be exploited in the design of self-powered devices for on-demand controlled drug and antidote delivery, and for sensing toxic substances in the environment (Nature Chem., 2014; Adv. Func. Mater., 2016)
  • Emergent swarming and predator-prey behavior based on chemotaxis occurs for particles and enzyme molecules that produce self-generated chemical gradients. Controlled formation of zones of attraction and exclusion, as well as spatio-temporal reversibility, can be achieved (J. Am. Chem. Soc., 2013, 2013).
  • Trisegmented Au-Ru-Au and Ru-Au-Ru rods trigger electrokinetic fluid pumping along their axis as “pullers” and “pushers”, respectively. Simulations and experiments with passive tracer particles show that catalytically generated hydrodynamic and electrostatic forces both contribute to pairwise and collective particle assembly (Soft Matter, 2016).
  • 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 (Nature Commun., 2015).
  • Chemically-driven convective flows leading to transport in and out of dead-end pores can occur, 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 (ACS Nano, 2015).
  • 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. (ACS Nano, 2014).
  •  “Acoustic tweezers” have been developed to manipulate particles, cells, and organisms. The acoustic tweezers technology is capable of delivering high-precision, high-throughput, high-efficiency cell/particle/organism manipulation in a simple, inexpensive, cell-phone-sized device (Proc. Nat. Acad. Sci., 2014, 2015, 2015, 2016).

Publications

A. Nourhani, V. H. Crespi, P.E. Lammert, “Guiding Chiral Self-Propellers in a Periodic Potential”, Phys. Rev. Lett., 115, 118101, (2015)

A. Nourhani, V. H. Crespi, P.E. Lammert, “Self-Consistent Nonlocal Feedback Theory for Electrocatalytic Swimmers with Heterogeneous Surface Chemical Kinetics, Phys. Rev. E, 91, 062303 (2015)

D. Ahmed, M. Lu, A. Nourhani, P.E. Lammert, Z. Stratton, H.S. Muddana, V. H. Crespi, T.J. Huang, “Selectively Manipulable Acoustic-Powered Microswimmers”, Scientific Reports, 5, 9744 (2015)

A. Nourhani, V. H. Crespi, P.E. Lammert, A. Borhan, “Self-Electrophoresis of Spheroidal Electrocatalytic Swimmers”, Phys. Fluids, 27, 092002, (2015)

Yazdi, S., Ardekani, A. M., and Borhan, A., “Swimming dynamics near a wall in a weakly elastic fluid,” J. Nonlinear Sci. 25 (5), 1153-1167, (2015)

A. Nourhani, P.E. Lammert, V. H. Crespi, A. Borhan, “A general Flux-Based Analysis for Spherical Electrocatalytic Nanomotors”, Phys. Fluids, 27, 012001 (2015)

Wei Wang, Wentao Duan, Zexin Zhang, Mei Sun, Ayusman Sen, and Thomas E. Mallouk, “A Tale of Two Forces: Simultaneous Chemical and Acoustic Propulsion of Bimetallic Micromotors,” Chemical Commun., 51, 1020, (DOI:10.1039/C4CC09149C) (2015)

Vinita Yadav, Wentao Duan, and Ayusman Sen, “Diffusiophoretic Nano and Microscale Propulsion and Communication,” In “Engineering of Chemical Complexity,” World Scientific Lecture Notes in Complex Systems, 12, 73, (2015)

Peter J. Butler, Krishna K. Dey, and Ayusman Sen, “Impulsive Enzymes: A New Force in Mechanobiology,” Cellular and Molecular Bioengineering, 8, 106, (DOI:10.1007/s12195-014-0376-1) (2015)

Wei Wang, Wentao Duan, Suzanne Ahmed, Ayusman Sen, and Thomas E. Mallouk, “From One to Many: Dynamic Assembly and Collective Behavior of Self-Propelled Colloidal Motors,” Acc. Chem. Res., 48, 1938, (DOI:10.1021/acs.accounts.5b00025) (2015)

Wentao Duan, Wei Wang, Sambeeta Das, Vinita Yadav, Thomas E. Mallouk, and Ayusman Sen, “Synthetic Nano- and Micromachines in Analytical Chemistry: Sensing, Migration, Capture, Delivery, and Separation,” Annu. Rev. Anal. Chem., 8, 311, (DOI: 10.1146/annurev-anchem-071114-040125) (2015)

Vinita Yadav, Wentao Duan, Peter J. Butler, and Ayusman Sen, “Anatomy of Nanoscale Propulsion,”, Annu. Rev. Biophys, 44, 77, (DOI: 10.1146/annurev-biophys-060414-034216) (2015) Sambeeta Das, Astha Garg, Andrew I. Campbell, Jonathan Howse, Ayusman Sen, Darrell Velegol, Ramin Golestanian, and Stephen J. Ebbens, “Boundaries Can Steer Active Janus Spheres,” Nature Commun., (DOI: 10.1038/ncomms9999) (2015)

Golestanian, R. “Enhanced Diffusion of Enzymes that Catalyze Exothermic Reactions” Phys. Rev. Lett. 2015, 115, 108102. (2015)

Daniel Ahmed, Mengqian Lu, Amir Nourhani, Paul E. Lammert, Zak Stratton, Hari S. Muddanna, Vincent H. Crespi, and Tony Jun Huang, “Selectively manipulable acoustic-powered microswimmers”, Scientific Reports, Vol. 5, 9744, (2015)

Liqiang Ren, Yuchao Chen, Peng Li, Zhangming Mao, Po-Hsun Huang, Joseph Rufo, Feng Guo, Lin Wang, J. Philip McCoy, Stewart J. Levine, and Tony Jun Huang, “A high-throughput acoustic cell sorter”, Lab on a Chip, Vol. 15, pp. 3870-3879 (2015)

Yuliang Xie, Chandraprakash Chindam, Nitesh Nama, Shikuan Yang, Mengqian Lu, Yanhui Zhao, John D. Mai, Francesco Costanzo, and Tony Jun Huang, “Exploring bubble oscillation and mass transfer enhancements in acoustic-assisted liquid-liquid extraction with a microfluidic device”, Scientific Reports, Vol. 5, pp. 12572, (2015)

Mingsong Wang, Chenglong Zhao, Xiaoyu Miao, Yanhui Zhao, Joseph Rufo, Yan Jun Liu, Tony Jun Huang, and Yuebing Zheng, “Plasmofluidics: Merging Light and Fluids at the Micro-/Nano-Scale”, Small, Vol. 11, 35, pp. 4423–4444 (2015)

Daniel Ahmed, Xiaolei Peng, Adem Ozcelik, Yuebing Zheng, Tony Jun Huang, “Acousto-Plasmofluidics: Acoustic Modulation of Surface Plasmon Resonance in Microfluidic Systems”, AIP Advances, Vol. 5, pp. 097161, (2015)

Nitesh Nama, Rune Barnkob, Zhangming Mao, Christian J. Kähler, Francesco Costanzo, and Tony Jun Huang, “Numerical study of acoustophoretic motion of particles in a PDMS microchannel driven by surface acoustic waves”, Lab on a Chip, Vol. 15, pp. 2700-2709, (2015)

Feng Guo, Weijie Zhou, Peng Li, Zhangming Mao, Neela Yennawar, Jarrod B. French, and Tony Jun Huang, “Precise Manipulation and Patterning of Protein Crystals for Macromolecular Crystallography using Surface Acoustic Waves”, Small, Vol. 11 (23), pp. 2733–2737 (2015)

Peng Li, Zhangming Mao, Zhangli Peng, Lanlan Zhou, Yuchao Chen, Po-Hsun Huang, Cristina I. Truica, Joseph J. Drabick, Wafik S. El-Deiry, Ming Dao, Subra Suresh, and Tony Jun Huang, “Acoustic Separation of Circulating Tumor Cells”, Proceedings of the National Academy of Sciences of the United States of America (PNAS), Vol. 112 (16), pp. 4970–4975, (2015)

Feng Guo, Peng Li, Jarrod B. French, Zhangming Mao, Hong Zhao, Sixing Li, Nitesh Nama, James R. Fick, Stephen J. Benkovic, and Tony Jun Huang, “Controlling Cell-Cell Interactions using Surface Acoustic Waves”, Proceedings of the National Academy of Sciences of the United States of America (PNAS), Vol. 112, pp. 43–48, (2015)

Sixing Li, Xiaoyun Ding, Zhangming Mao, Yuchao Chen, Nitesh Nama, Feng Guo, Peng Li, Lin Wang, Craig E. Cameron and Tony Jun Huang, “Standing surface acoustic wave (SSAW)-based cell washing”, Lab on a Chip, Vol. 15, pp. 331-338, (2015)

Zhangming Mao, Feng Guo, Yuliang Xie, Yanhui Zhao, Michael Ian Lapsley, Lin Wang, John D. Mai, Francesco Costanzo, and Tony Jun Huang,”* Label-free measurements of reaction kinetics using a droplet-based optofluidic device”, Journal of Laboratory Automation, Vol. 20, pp. 17-24 (2015)

Abhishek Kar, Tso-Yi Chiang, Isamar Ortiz Rivera, Ayusman Sen, and Darrell Velegol, “Enhanced Transport Into and Out of Dead-End Pores,” ACS Nano, 9, 746 (DOI:10.1021/nn506216b) (2015)

T.-Y. Chiang and D. Velegol, "Multi-ion diffusiophoresis," J. Coll. Interf. Sci. 2014, 424, 120-123.

S. Ahmed, D. Gentekos, C. A. Fink, and T. E. Mallouk, "Self-assembly of nanorod motors into geometrically regular multimers and their propulsion by ultrasound," i>ACS Nano, 2014, 8, 11053-11060.

A. Kar, R. Guha, N. Dani, and D. Velegol, "Particle Deposition on Microporous Membranes Can Be Enhanced or Reduced by Salt Gradients," Langmuir, 2014, 30, 793-799.

A. Balk, L. Mair, P. Mathai, P. Patrone, W. Wang, S. Ahmed, T. E. Mallouk, J. A. Liddle, and S. Stavis, "Kilohertz rotation of nanomotors propelled by ultrasound traced by microvortex advection of nanoparticles," ACS Nano, 2014, 8, 8300-8309.

V. Yadav, R. A. Pavlick, S. M. Meckler, and A. Sen, “Triggered Detection and Deposition: Toward the Repair of Microcracks,” Chem. Mater., 2014, 26, 4647.

T.-Y. Chiang and D. Velegol, "Localized Electroosmosis (LEO) Induced by Spherical Colloidal Motors," Langmuir, 2014, 30, 2600-2607.

S. Sengupta, .M M. Spiering, K. K. Dey, W. Duan, D. Patra, P. J. Butler, R. D. Astumian, S. J. Benkovic, and A, Sen, “DNA Polymerase as a Molecular Motor and Pump,” ACS Nano, 2014, 8, 2410.

S. Sengupta, D. Patra, I. O. Rivera, A. Agrawal, K. K. Dey, S. Shklyaev, T. E. Mallouk, and A. Sen, "Self-Powered Enzyme Micropumps," Nature Chem., 6, 415.

W. Wang, W. Duan, S. Ahmed, T. E. Mallouk, and A. Sen, "Small power: autonomous nano- and micromotors propelled by self-generated gradients," Nano Today, 2013, 5, 531-554.

W. Wang, W. Duan, A. Sen, and T. E. Mallouk, "Catalytically-powered dynamic assembly of rod-shaped nanomotors and passive tracer particles," PNAS, 2013, 110, 17744-17749.

V. Yadav, J. D. Freedman, M. Grinstaff, and A. Sen, "Bone-Crack Detection, Targeting, and Repair Using Ion Gradients," Angew. Chem., Int. Ed., 2013, 52, 10997-11001.

D. Patra, H. Zhang, S. Sengupta, and A. Sen, "Dual Stimuli-Responsive, Rechargeable Micropumps via "Host-Guest" Interactions," ACS Nano, 2013, 7, 7674.

M. S. Baker, V. Yadav, A. Sen, and S. T. Phillips, "A Self-Powered Polymeric Material that Responds Autonomously and Continuously to Fleeting Stimuli," Angew. Chem., Int. Ed., 2013, 52, 10295

A. M. DiLauro, H. Zhang, M. S. Baker, F. Wong, A. Sen, and S. T. Phillips, "Accessibility of Responsive End-Caps in Films Composed of Stimuli-Responsive, Depolymerizable Poly(phthalaldehydes)," Macromolecules, 2013, 46, 7257

W. Wang, T.-Y. Chiang, D. Velegol, and T. E. Mallouk, "Understanding the Efficiency of Autonomous Nano- and Micromotors" J. Am. Chem. Soc., 135, 10557-65 (2013).

D. Ahmed, C. Y. Chan, S. S. Lin, H. S. Muddana, N. Nama, and T. J. Huang, "Tunable, Pulsatile Chemical Gradient Generation via Acoustically Driven Oscillating Bubbles," Lab on a Chip, 13, 328-331 (2013).

W. Duan, R. Liu, and A. Sen, "Transition between Collective Behaviors of Micromotors in Response to Different Stimuli," Journal of the American Chemical Society, 135, 1280 (2013).

S. Yang, M. I. Lapsley, B. Cao, C. Zhao, Y. Zhao, Q. Hao, B. Kiraly, J. Scott, W. Li, L. Wang, Y. Lei, and T. J. Huang, "Large-Scale Fabrication of Three-Dimensional Surface Patterns Using Template-Defined Electrochemical Deposition," Advanced Functional Materials, 23, 720-730 (2013).

Q. Hao, S. Morton, B. Wang, Y. Zhao, L. Jensen, and T. J. Huang, "Tuning Surface-Enhanced Raman Scattering from Graphene Substrates using the Electric Field Effect and Chemical Doping," Applied Physics Letters, 102, 011102 (2013).

R. A. Pavlick, K. K. Dey, A. Sirjoosingh, A. Benesi, and A. Sen, "A catalytically driven organometallic molecular motor" Nanoscale, 2013, 5, 1301-1304.

Y. Chen, X. Ding, S.-C. S. Lin, S. Yang, P.-H. Huang, N. Nama, Y. Zhao, A. A. Nawaz, F. Guo, W. Wang, T. E. Mallouk, and T. J. Huang, "Tunable nanowire patterning using standing surface acoustic waves (SSAW)" ACS Nano, 7, 3306-14 (2013).

S. Sengupta, K. K. Dey, H. S. Muddana, T. Tabouillot, M. E. Ibele, P. J. Butler, and A. Sen, "Enzyme Molecules as Nanomotors," Journal of the American Chemical Society, 135, 1406 (2013).