Publications by Ramin Golestanian

Magnetically-actuated artificial cilium: a simple theoretical model.

Soft matter (2019)

F Meng, D Matsunaga, JM Yeomans, R Golestanian

We propose a theoretical model for a magnetically-actuated artificial cilium in a fluid environment and investigate its dynamical behaviour, using both analytical calculations and numerical simulations. The cilium consists of a spherical soft magnet, a spherical hard magnet, and an elastic spring that connects the two magnetic components. Under a rotating magnetic field, the cilium exhibits a transition from phase-locking at low frequencies to phase-slipping at higher frequencies. We study the dynamics of the magnetic cilium in the vicinity of a wall by incorporating its hydrodynamic influence, and examine the efficiency of the actuated cilium in pumping viscous fluids. This cilium model can be helpful in a variety of applications such as transport and mixing of viscous solutions at small scales and fabricating microswimmers.

Chemical and hydrodynamic alignment of an enzyme.

The Journal of chemical physics 150 (2019) 115102-

T Adeleke-Larodo, J Agudo-Canalejo, R Golestanian

Motivated by the implications of the complex and dynamic modular geometry of an enzyme on its motion, we investigate the effect of combining long-range internal and external hydrodynamic interactions due to thermal fluctuations with short-range surface interactions. An asymmetric dumbbell consisting of two unequal subunits, in a nonuniform suspension of a solute with which it interacts via hydrodynamic interactions as well as non-contact surface interactions, is shown to have two alignment mechanisms due to the two types of interactions. In addition to alignment, the chemical gradient results in a drift velocity that is modified by hydrodynamic interactions between the constituents of the enzyme.

Phoresis and Enhanced Diffusion Compete in Enzyme Chemotaxis.

Nano letters 18 (2018) 2711-2717

J Agudo-Canalejo, P Illien, R Golestanian

Chemotaxis of enzymes in response to gradients in the concentration of their substrate has been widely reported in recent experiments, but a basic understanding of the process is still lacking. Here, we develop a microscopic theory for chemotaxis that is valid for enzymes and other small molecules. Our theory includes both nonspecific interactions between enzyme and substrate as well as complex formation through specific binding between the enzyme and the substrate. We find that two distinct mechanisms contribute to enzyme chemotaxis: a diffusiophoretic mechanism due to the nonspecific interactions and a new type of mechanism due to binding-induced changes in the diffusion coefficient of the enzyme. The latter chemotactic mechanism points toward lower substrate concentration if the substrate enhances enzyme diffusion and toward higher substrate concentration if the substrate inhibits enzyme diffusion. For a typical enzyme, attractive phoresis and binding-induced enhanced diffusion will compete against each other. We find that phoresis dominates above a critical substrate concentration, whereas binding-induced enhanced diffusion dominates for low substrate concentration. Our results resolve an apparent contradiction regarding the direction of urease chemotaxis observed in experiments and, in general, clarify the relation between the enhanced diffusion and the chemotaxis of enzymes. Finally, we show that the competition between the two distinct chemotactic mechanisms may be used to engineer nanomachines that move toward or away from regions with a specific substrate concentration.

Enhanced Diffusion and Chemotaxis at the Nanoscale.

Accounts of chemical research 51 (2018) 2365-2372

J Agudo-Canalejo, T Adeleke-Larodo, P Illien, R Golestanian

Enzymes have been recently proposed to have mechanical activity associated with their chemical activity. In a number of recent studies, it has been reported that enzymes undergo enhanced diffusion in the presence of their corresponding substrate when this substrate is uniformly distributed in solution. Moreover, if the concentration of the substrate is nonuniform, enzymes and other small molecules have been reported to show chemotaxis (biased stochastic movement in the direction of the substrate gradient), typically toward higher concentrations of this substrate, with a few exceptions. The underlying physical mechanisms responsible for enhanced diffusion and chemotaxis at the nanoscale, however, are still not well understood. Understanding these processes is important both for fundamental biological research, for example, in the context of spatial organization of enzymes in metabolic pathways (metabolon formation), as well as for engineering applications, such as in the design of new vehicles for targeted drug delivery. In this Account, we will review the available experimental observations of both enhanced diffusion and chemotaxis, and we will discuss critically the different theories that have been proposed to explain the two. We first focus on enhanced diffusion, beginning with an overview of the experimental results. We then discuss the two main types of mechanisms that have been proposed, namely, active mechanisms relying on the catalytic step of the enzymatic reaction and equilibrium mechanisms, which consider the reversible binding and unbinding of the substrate to the enzyme. We put particular emphasis on an equilibrium model recently introduced by us, which describes how the diffusion of dumbbell-like modular enzymes can be enhanced in the presence of substrate thanks to a binding-induced reduction of the internal fluctuations of the enzyme. We then turn to chemotaxis, beginning with an overview of the experimental evidence for the chemotaxis of enzymes and small molecules, followed by a description of a number of shortcomings and pitfalls in the thermodynamic and phenomenological models for chemotaxis introduced in those and other works in the literature. We then discuss a microscopic model for chemotaxis including both noncontact interactions and specific binding between enzyme and substrate recently developed by us, which overcomes many of these shortcomings and is consistent with the experimental observations of chemotaxis. Finally, we show that the results of this model may be used to engineer chemically active macromolecules that are directed in space via patterning of the concentrations of their substrates.

Current fluctuations across a nano-pore.

Journal of physics. Condensed matter : an Institute of Physics journal 30 (2018) 134001-

M Zorkot, R Golestanian

The frequency-dependent spectrum of current fluctuations through nano-scale channels is studied using analytical and computational techniques. Using a stochastic Nernst-Planck description and neglecting the interactions between the ions inside the channel, an expression is derived for the current fluctuations, assuming that the geometry of the channel can be incorporated through the lower limits for various wave-vector modes. Since the resulting expression turns out to be quite complex, a number of further approximations are discussed such that relatively simple expressions can be used for practical purposes. The analytical results are validated using Langevin dynamics simulations.

Shape dependent phoretic propulsion of slender active particles


Y Ibrahim, R Golestanian, TB Liverpool

Clustering of Magnetic Swimmers in a Poiseuille Flow.

Physical review letters 120 (2018) 188101-

F Meng, D Matsunaga, R Golestanian

We investigate the collective behavior of magnetic swimmers, which are suspended in a Poiseuille flow and placed under an external magnetic field, using analytical techniques and Brownian dynamics simulations. We find that the interplay between intrinsic activity, external alignment, and magnetic dipole-dipole interactions leads to longitudinal structure formation. Our work sheds light on a recent experimental observation of a clustering instability in this system.

Multigenerational memory and adaptive adhesion in early bacterial biofilm communities.

Proceedings of the National Academy of Sciences of the United States of America 115 (2018) 4471-4476

CK Lee, J de Anda, AE Baker, RR Bennett, Y Luo, EY Lee, JA Keefe, JS Helali, J Ma, K Zhao, R Golestanian, GA O'Toole, GCL Wong

Using multigenerational, single-cell tracking we explore the earliest events of biofilm formation by Pseudomonas aeruginosa During initial stages of surface engagement (≤20 h), the surface cell population of this microbe comprises overwhelmingly cells that attach poorly (∼95% stay <30 s, well below the ∼1-h division time) with little increase in surface population. If we harvest cells previously exposed to a surface and direct them to a virgin surface, we find that these surface-exposed cells and their descendants attach strongly and then rapidly increase the surface cell population. This "adaptive," time-delayed adhesion requires determinants we showed previously are critical for surface sensing: type IV pili (TFP) and cAMP signaling via the Pil-Chp-TFP system. We show that these surface-adapted cells exhibit damped, coupled out-of-phase oscillations of intracellular cAMP levels and associated TFP activity that persist for multiple generations, whereas surface-naïve cells show uncorrelated cAMP and TFP activity. These correlated cAMP-TFP oscillations, which effectively impart intergenerational memory to cells in a lineage, can be understood in terms of a Turing stochastic model based on the Pil-Chp-TFP framework. Importantly, these cAMP-TFP oscillations create a state characterized by a suppression of TFP motility coordinated across entire lineages and lead to a drastic increase in the number of surface-associated cells with near-zero translational motion. The appearance of this surface-adapted state, which can serve to define the historical classification of "irreversibly attached" cells, correlates with family tree architectures that facilitate exponential increases in surface cell populations necessary for biofilm formation.

Far-field theory for trajectories of magnetic ellipsoids in rectangular and circular channels


D Matsunaga, A Zottl, F Meng, R Golestanian, JM Yeomans

High-Speed "4D" Computational Microscopy of Bacterial Surface Motility

ACS NANO 11 (2017) 9340-9351

J de Anda, EY Lee, CK Lee, RR Bennett, X Ji, S Soltani, MC Harrison, AE Baker, Y Luo, T Chou, GA O'Toole, AM Armani, R Golestanian, GCL Wong

High-Speed "4D" Computational Microscopy of Bacterial Surface Motility.

ACS nano 11 (2017) 9340-9351

J de Anda, EY Lee, CK Lee, RR Bennett, X Ji, S Soltani, MC Harrison, AE Baker, Y Luo, T Chou, GA O'Toole, AM Armani, R Golestanian, GCL Wong

Bacteria exhibit surface motility modes that play pivotal roles in early-stage biofilm community development, such as type IV pili-driven "twitching" motility and flagellum-driven "spinning" and "swarming" motility. Appendage-driven motility is controlled by molecular motors, and analysis of surface motility behavior is complicated by its inherently 3D nature, the speed of which is too fast for confocal microscopy to capture. Here, we combine electromagnetic field computation and statistical image analysis to generate 3D movies close to a surface at 5 ms time resolution using conventional inverted microscopes. We treat each bacterial cell as a spherocylindrical lens and use finite element modeling to solve Maxwell's equations and compute the diffracted light intensities associated with different angular orientations of the bacterium relative to the surface. By performing cross-correlation calculations between measured 2D microscopy images and a library of computed light intensities, we demonstrate that near-surface 3D movies of Pseudomonas aeruginosa translational and rotational motion are possible at high temporal resolution. Comparison between computational reconstructions and detailed hydrodynamic calculations reveals that P. aeruginosa act like low Reynolds number spinning tops with unstable orbits, driven by a flagellum motor with a torque output of ∼2 pN μm. Interestingly, our analysis reveals that P. aeruginosa can undergo complex flagellum-driven dynamical behavior, including precession, nutation, and an unexpected taxonomy of surface motility mechanisms, including upright-spinning bacteria that diffuse laterally across the surface, and horizontal bacteria that follow helicoidal trajectories and exhibit superdiffusive movements parallel to the surface.

Diffusion of an enzyme: The role of fluctuation-induced hydrodynamic coupling

EPL 119 (2017) ARTN 40002

P Illien, T Adeleke-Larodo, R Golestanian

Synchronization and Collective Dynamics of Flagella and Cilia as Hydrodynamically Coupled Oscillators


N Uchida, R Golestanian, RR Bennett

Division for multiplication

NATURE PHYSICS 13 (2017) 323-324

R Golestanian

Exothermicity Is Not a Necessary Condition for Enhanced Diffusion of Enzymes.

Nano letters 17 (2017) 4415-4420

P Illien, X Zhao, KK Dey, PJ Butler, A Sen, R Golestanian

Recent experiments have revealed that the diffusivity of exothermic and fast enzymes is enhanced when they are catalytically active, and different physical mechanisms have been explored and quantified to account for this observation. We perform measurements on the endothermic and relatively slow enzyme aldolase, which also shows substrate-induced enhanced diffusion. We propose a new physical paradigm, which reveals that the diffusion coefficient of a model enzyme hydrodynamically coupled to its environment increases significantly when undergoing changes in conformational fluctuations in a substrate concentration dependent manner, and is independent of the overall turnover rate of the underlying enzymatic reaction. Our results show that substrate-induced enhanced diffusion of enzyme molecules can be explained within an equilibrium picture and that the exothermicity of the catalyzed reaction is not a necessary condition for the observation of this phenomenon.

Shape of the growing front of biofilms


X Wang, HA Stone, R Golestanian

Frontiers of chaotic advection


H Aref, JR Blake, M Budisic, SSS Cardoso, JHE Cartwright, HJH Clercx, K El Omari, U Feudel, R Golestanian, E Gouillart, GF van Heijst, TS Krasnopolskaya, Y Le Guer, RS MacKay, VV Meleshko, G Metcalfe, I Mezic, APS de Moura, O Piro, MFM Speetjens, R Sturman, J-L Thiffeault, I Tuval

'Fuelled' motion: phoretic motility and collective behaviour of active colloids.

Chemical Society reviews 46 (2017) 5508-5518

P Illien, R Golestanian, A Sen

Designing microscopic and nanoscopic self-propelled particles and characterising their motion have become a major scientific challenge over the past few decades. To this purpose, phoretic effects, namely propulsion mechanisms relying on local field gradients, have been the focus of many theoretical and experimental studies. In this review, we adopt a tutorial approach to present the basic physical mechanisms at stake in phoretic motion, and describe the different experimental works that led to the fabrication of active particles based on this principle. We also present the collective effects observed in assemblies of interacting active colloids, and the theoretical tools that have been used to describe phoretic and hydrodynamic interactions.

Multiple phoretic mechanisms in the self-propulsion of a Pt-insulator Janus swimmer


Y Ibrahim, R Golestanian, TB Liverpool

Pattern formation by curvature-inducing proteins on spherical membranes


J Agudo-Canalejo, R Golestanian