Publications by Ramin Golestanian

Publisher's Note: "Chemical and hydrodynamic alignment of an enzyme" [J. Chem. Phys. 150, 115102 (2019)].

The Journal of chemical physics 150 (2019) 159903-

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

Experimental observation of flow fields around active Janus spheres.

Nature communications 10 (2019) 3952-

AI Campbell, SJ Ebbens, P Illien, R Golestanian

The phoretic mechanisms at stake in the propulsion of asymmetric colloids have been the subject of debates during the past years. In particular, the importance of electrokinetic effects on the motility of Pt-PS Janus sphere was recently discussed. Here, we probe the hydrodynamic flow field around a catalytically active colloid using particle tracking velocimetry both in the freely swimming state and when kept stationary with an external force. Our measurements provide information about the fluid velocity in the vicinity of the surface of the colloid, and confirm a mechanism for propulsion that was proposed recently. In addition to offering a unified understanding of the nonequilibrium interfacial transport processes at stake, our results open the way to a thorough description of the hydrodynamic interactions between such active particles and understanding their collective dynamics.

Flagella-like Beating of a Single Microtubule.

Nano letters 19 (2019) 3359-3363

A Vilfan, S Subramani, E Bodenschatz, R Golestanian, I Guido

Kinesin motors can induce a buckling instability in a microtubule with a fixed minus end. Here we show that by modifying the surface with a protein-repellent functionalization and using clusters of kinesin motors, the microtubule can exhibit persistent oscillatory motion resembling the beating of sperm flagella. The observed period is of the order of 1 min. From the experimental images we theoretically determine a distribution of motor forces that explains the observed shapes using a maximum likelihood approach. A good agreement is achieved with a small number of motor clusters acting simultaneously on a microtubule. The tangential forces exerted by a cluster are mostly in the range 0-8 pN toward the microtubule minus end, indicating the action of 1 or 2 kinesin motors. The lateral forces are distributed symmetrically and mainly below 10 pN, while the lateral velocity has a strong peak around zero. Unlike well-known models for flapping filaments, kinesins are found to have a strong "pinning" effect on the beating filaments. Our results suggest new strategies to utilize molecular motors in dynamic roles that depend sensitively on the stress built-up in the system.

Efficiency limits of the three-sphere swimmer

Physical Review Fluids 4 (2019)

B Nasouri, A Vilfan, R Golestanian

© 2019 American Physical Society. We consider a swimmer consisting of a collinear assembly of three spheres connected by two slender rods. This swimmer can propel itself forward by varying the lengths of the rods in a way that is not invariant under time reversal. Although any non-reciprocal strokes of the arms can lead to a net displacement, the energetic efficiency of the swimmer is strongly dependent on the details and sequences of these strokes, and also the sizes of the spheres. We define the efficiency of the swimmer using Lighthill's criterion, i.e., the power that is needed to pull the swimmer by an external force at a certain speed, divided by the power needed for active swimming with the same average speed. Here, we determine numerically the optimal stroke sequences and the optimal size ratio of the spheres, while limiting the maximum extension of the rods. Our calculation takes into account both far-field and near-field hydrodynamic interactions. We show that, surprisingly, the three-sphere swimmer with unequal spheres can be more efficient than the equally sized case. We also show that the variations of efficiency with size ratio is not monotonic and there exists a specific size ratio at which the swimmer has the highest efficiency. We find that the swimming efficiency initially rises by increasing the maximum allowable extension of the rods, and then converges to a maximum value. We calculate this upper limit analytically and report the highest value of efficiency that the three-sphere swimmer can reach.

Active Phase Separation in Mixtures of Chemically Interacting Particles.

Physical review letters 123 (2019) 018101-

J Agudo-Canalejo, R Golestanian

We theoretically study mixtures of chemically interacting particles, which produce or consume a chemical to which they are attracted or repelled, in the most general case of many coexisting species. We find a new class of active phase separation phenomena in which the nonequilibrium chemical interactions between particles, which break action-reaction symmetry, can lead to separation into phases with distinct density and stoichiometry. Because of the generic nature of our minimal model, our results shed light on the underlying fundamental principles behind nonequilibrium self-organization of cells and bacteria, catalytic enzymes, or phoretic colloids.

Active phase separation in mixtures of chemically-interacting particles


J Agudo-Canalejo, R Golestanian

Active phase separation in mixtures of chemically-interacting particles


J Agudo-Canalejo, R Golestanian

Controlling collective rotational patterns of magnetic rotors.

Nature communications 10 (2019) 4696-

D Matsunaga, JK Hamilton, F Meng, N Bukin, EL Martin, FY Ogrin, JM Yeomans, R Golestanian

Magnetic actuation is widely used in engineering specific forms of controlled motion in microfluidic applications. A challenge, however, is how to extract different desired responses from different components in the system using the same external magnetic drive. Using experiments, simulations, and theoretical arguments, we present emergent rotational patterns in an array of identical magnetic rotors under an uniform, oscillating magnetic field. By changing the relative strength of the external field strength versus the dipolar interactions between the rotors, different collective modes are selected by the rotors. When the dipole interaction is dominant the rotors swing upwards or downwards in alternating stripes, reflecting the spin-ice symmetry of the static configuration. For larger spacings, when the external field dominates over the dipolar interactions, the rotors undergo full rotations, with different quarters of the array turning in different directions. Our work sheds light on how collective behaviour can be engineered in magnetic systems.

Pairing, waltzing and scattering of chemotactic active colloids


S Saha, S Ramaswamy, R Golestanian

Bose-Einstein-like condensation in scalar active matter with diffusivity edge

Physical Review E 100 (2019)

R Golestanian

© 2019 American Physical Society. Due to their remarkable properties, systems that exhibit self-organization of their components resulting from intrinsic microscopic activity have been extensively studied in the last two decades. In a generic class of active matter, the interactions between the active components are represented via an effective density-dependent diffusivity in a mean-field single-particle description. Here, a class of scalar active matter is proposed by incorporating a diffusivity edge into the dynamics: when the local density of the system surpasses a critical threshold, the diffusivity vanishes. The effect of the diffusivity edge is studied under the influence of an external potential, which introduces the ability to control the behavior of the system by changing an effective temperature, which is defined in terms of the single-particle diffusivity and mobility. At a critical effective temperature, a system that is trapped by a harmonic potential is found to undergo a condensation transition, which manifests formal similarities to Bose-Einstein condensation.

Magnetically-actuated artificial cilium: a simple theoretical model.

Soft matter 15 (2019) 3864-3871

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.

Fluctuation-induced hydrodynamic coupling in an asymmetric, anisotropic dumbbell.

The European physical journal. E, Soft matter 42 (2019) 39-

T Adeleke-Larodo, P Illien, R Golestanian

We recently introduced a model of an asymmetric dumbbell made of two hydrodynamically coupled subunits as a minimal model for a macromolecular complex, in order to explain the observation of enhanced diffusion of catalytically active enzymes. It was shown that internal fluctuations lead to a negative contribution to the overall diffusion coefficient and that the fluctuation-induced contribution is controlled by the strength of the interactions between the subunits and their asymmetry. We develop the model by studying the effect of anisotropy on the diffusion properties of a modular structure. Using a moment expansion method we derive an analytic form for the long-time diffusion coefficient of an asymmetric, anisotropic dumbbell and show systematically its dependence on internal and external symmetry. The method provides a tractable, analytical route for studying the stochastic dynamics of dumbbell models. The present work opens the way to more detailed descriptions of the effect of hydrodynamic interactions on the diffusion and transport properties of biomolecules with complex structures.

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.

Trail-mediated self-interaction.

The Journal of chemical physics 150 (2019) 214111-

WT Kranz, R Golestanian

A number of microorganisms leave persistent trails while moving along surfaces. For single-cell organisms, the trail-mediated self-interaction will influence the dynamics. It has been discussed recently [Kranz et al., Phys. Rev. Lett. 117, 038101 (2016)] that the self-interaction may localize the organism above a critical coupling χc to the trail. Here, we will derive a generalized active particle model capturing the key features of the self-interaction and analyze its behavior for smaller couplings χ < χc. We find that fluctuations in propulsion speed shift the localization transition to stronger couplings.

Tunable self-healing of magnetically propelling colloidal carpets.

Nature communications 10 (2019) 2444-

H Massana-Cid, F Meng, D Matsunaga, R Golestanian, P Tierno

The process of crystallization is difficult to observe for transported, out-of-equilibrium systems, as the continuous energy injection increases activity and competes with ordering. In emerging fields such as microfluidics and active matter, the formation of long-range order is often frustrated by the presence of hydrodynamics. Here we show that a population of colloidal rollers assembled by magnetic fields into large-scale propelling carpets can form perfect crystalline materials upon suitable balance between magnetism and hydrodynamics. We demonstrate a field-tunable annealing protocol based on a controlled colloidal flow above the carpet that enables complete crystallization after a few seconds of propulsion. The structural transition from a disordered to a crystalline carpet phase is captured via spatial and temporal correlation functions. Our findings unveil a novel pathway to magnetically anneal clusters of propelling particles, bridging driven systems with crystallization and freezing in material science.

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.

Control of synchronization in models of hydrodynamically coupled motile cilia

Communications Physics 1 (2018)

A Maestro, N Bruot, J Kotar, N Uchida, R Golestanian, P Cicuta

© 2018, The Author(s). In many organisms, multiple motile cilia coordinate their beating to facilitate swimming or driving of surface flows. Simple models are required to gain a quantitative understanding of how such coordination is achieved; there are two scales of phenomena, within and between cilia, and both host complex non-linear and non-thermal effects. We study here a model that is tractable analytically and can be realized by optical trapping colloidal particles: intra-cilia properties are coarse grained into the parameters chosen to drive particles around closed local orbits. Depending on these effective parameters a variety of phase-locked steady states can be achieved. We derive a theory that includes two mechanisms for synchronization: the flexibility of the motion along the predefined orbit and the modulation of the driving force. We show that modest tuning of the cilia beat properties, as could be achieved biologically, results in dramatic changes in the collective motion arising from hydrodynamic coupling.

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.

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