Publications by Ramin Golestanian

Cooperatively enhanced reactivity and "stabilitaxis" of dissociating oligomeric proteins.

Proceedings of the National Academy of Sciences of the United States of America 117 (2020) 11894-11900

J Agudo-Canalejo, P Illien, R Golestanian

Many functional units in biology, such as enzymes or molecular motors, are composed of several subunits that can reversibly assemble and disassemble. This includes oligomeric proteins composed of several smaller monomers, as well as protein complexes assembled from a few proteins. By studying the generic spatial transport properties of such proteins, we investigate here whether their ability to reversibly associate and dissociate may confer on them a functional advantage with respect to nondissociating proteins. In uniform environments with position-independent association-dissociation, we find that enhanced diffusion in the monomeric state coupled to reassociation into the functional oligomeric form leads to enhanced reactivity with localized targets. In nonuniform environments with position-dependent association-dissociation, caused by, for example, spatial gradients of an inhibiting chemical, we find that dissociating proteins generically tend to accumulate in regions where they are most stable, a process that we term "stabilitaxis."

Exact Phoretic Interaction of Two Chemically Active Particles.

Physical review letters 124 (2020) 168003-

B Nasouri, R Golestanian

We study the nonequilibrium interaction of two isotropic chemically active particles taking into account the exact near-field chemical interactions as well as hydrodynamic interactions. We identify regions in the parameter space wherein the dynamical system describing the two particles can have a fixed point-a phenomenon that cannot be captured under the far-field approximation. We find that, due to near-field effects, the particles may reach a stable equilibrium at a nonzero gap size or make a complex that can dissociate in the presence of sufficiently strong noise. We explicitly show that the near-field effects originate from a self-generated neighbor-reflected chemical gradient, similar to interactions of a self-propelling phoretic particle and a flat substrate.

The 2020 motile active matter roadmap.

Journal of physics. Condensed matter : an Institute of Physics journal 32 (2020) 193001-

G Gompper, RG Winkler, T Speck, A Solon, C Nardini, F Peruani, H Löwen, R Golestanian, UB Kaupp, L Alvarez, T Kiørboe, E Lauga, WCK Poon, A DeSimone, S Muiños-Landin, A Fischer, NA Söker, F Cichos, R Kapral, P Gaspard, M Ripoll, F Sagues, A Doostmohammadi, JM Yeomans, IS Aranson, C Bechinger, H Stark, CK Hemelrijk, FJ Nedelec, T Sarkar, T Aryaksama, M Lacroix, G Duclos, V Yashunsky, P Silberzan, M Arroyo, S Kale

Activity and autonomous motion are fundamental in living and engineering systems. This has stimulated the new field of 'active matter' in recent years, which focuses on the physical aspects of propulsion mechanisms, and on motility-induced emergent collective behavior of a larger number of identical agents. The scale of agents ranges from nanomotors and microswimmers, to cells, fish, birds, and people. Inspired by biological microswimmers, various designs of autonomous synthetic nano- and micromachines have been proposed. Such machines provide the basis for multifunctional, highly responsive, intelligent (artificial) active materials, which exhibit emergent behavior and the ability to perform tasks in response to external stimuli. A major challenge for understanding and designing active matter is their inherent nonequilibrium nature due to persistent energy consumption, which invalidates equilibrium concepts such as free energy, detailed balance, and time-reversal symmetry. Unraveling, predicting, and controlling the behavior of active matter is a truly interdisciplinary endeavor at the interface of biology, chemistry, ecology, engineering, mathematics, and physics. The vast complexity of phenomena and mechanisms involved in the self-organization and dynamics of motile active matter comprises a major challenge. Hence, to advance, and eventually reach a comprehensive understanding, this important research area requires a concerted, synergetic approach of the various disciplines. The 2020 motile active matter roadmap of Journal of Physics: Condensed Matter addresses the current state of the art of the field and provides guidance for both students as well as established scientists in their efforts to advance this fascinating area.

SerraNA: a program to determine nucleic acids elasticity from simulation data


V Velasco-Berrelleza, M Burman, J Shepherd, M Leake, R Golestanian, A Noy

Abstract The resistance of DNA to stretch, twist and bend is broadly well estimated by experiments and is important for gene regulation and chromosome packing. However, their sequence-dependence and how bulk elastic constants emerge from local fluctuations is less understood. Here, we present SerraNA , which is an open software that calculates elastic parameters of double-stranded nucleic acids from dinucleotide length up to the whole molecule using ensembles from numerical simulations. The program reveals that global bendability emerge from local periodic bending angles in phase with the DNA helicoidal shape. We also apply SerraNA to the whole set of 136 tetra-bp combinations and we observe a high degree of sequence-dependence for all elastic parameters with differences over 200%. Tetramers with TA and CA base-pair steps are especially flexible, while tetramers containing AA and AT tend to be the most rigid. Our results thus suggest AT-rich motifs generate extreme mechanical properties depending of the exact sequence ordering, which seems critical for creating strong global bendability on longer sequences when phased properly. SerraNA is a tool to be applied in the next generation of interdisciplinary investigations to further understand what determines the elasticity of DNA. <jats:sec id="s6"> Graphical TOC Entry <jats:fig id="ufig1" position="float" orientation="portrait" fig-type="figure"><jats:graphic xmlns:xlink="" xlink:href="004945v2_ufig1" position="float" orientation="portrait" />

Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of Pseudomonas aeruginosa PA14 and PAO1.

mBio 11 (2020)

CK Lee, J Vachier, J de Anda, K Zhao, AE Baker, RR Bennett, CR Armbruster, KA Lewis, RL Tarnopol, CJ Lomba, DA Hogan, MR Parsek, GA O'Toole, R Golestanian, GCL Wong

What are bacteria doing during "reversible attachment," the period of transient surface attachment when they initially engage a surface, besides attaching themselves to the surface? Can an attaching cell help any other cell attach? If so, does it help all cells or employ a more selective strategy to help either nearby cells (spatial neighbors) or its progeny (temporal neighbors)? Using community tracking methods at the single-cell resolution, we suggest answers to these questions based on how reversible attachment progresses during surface sensing for Pseudomonas aeruginosa strains PAO1 and PA14. Although PAO1 and PA14 exhibit similar trends of surface cell population increase, they show unanticipated differences when cells are considered at the lineage level and interpreted using the quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two surface colonization strategies. PAO1 lineages commit quickly to a surface compared to PA14 lineages, with early c-di-GMP-mediated exopolysaccharide (EPS) production that can facilitate the attachment of neighbors. PA14 lineages modulate their motility via cyclic AMP (cAMP) and retain memory of the surface so that their progeny are primed for improved subsequent surface attachment. Based on the findings of previous studies, we propose that the differences between PAO1 and PA14 are potentially rooted in downstream differences between Wsp-based and Pil-Chp-based surface-sensing systems, respectively.IMPORTANCE The initial pivotal phase of bacterial biofilm formation known as reversible attachment, where cells undergo a period of transient surface attachment, is at once universal and poorly understood. What is more, although we know that reversible attachment culminates ultimately in irreversible attachment, it is not clear how reversible attachment progresses phenotypically, as bacterial surface-sensing circuits fundamentally alter cellular behavior. We analyze diverse observed bacterial behavior one family at a time (defined as a full lineage of cells related to one another by division) using a unifying stochastic model and show that our findings lead to insights on the time evolution of reversible attachment and the social cooperative dimension of surface attachment in PAO1 and PA14 strains.

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 Springer Nature 10 (2019) 4696

D Matsunaga, JK Hamilton, F Meng, J Yeomans, R Golestanian

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) 010601-

R Golestanian

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 Royal Society of Chemistry (2019) 3864-3871

F Meng, D Matsunaga, J 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

European Physical Journal E Springer 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.

Phenotypic differences in reversible attachment behavior reveal distinct P. aeruginosa surface colonization strategies


C Lee, J Vachier, JD Anda, K Zhao, A Baker, R Bennett, C Armbruster, K Lewis, R Tarnopol, C Lomba, D Hogan, M Parsek, G O’Toole, R Golestanian, G Wong

Abstract Despite possessing the machinery to sense, adhere to, and proliferate on surfaces, it is commonly observed that bacteria initially have a difficult time attaching to a surface. Before forming a bacterial biofilm, planktonic bacteria exhibit a random period of transient surface attachment known as “reversible attachment” which is poorly understood. Using community tracking methods at single-cell resolution, we examine how reversible attachment progresses during initial stages of surface sensing. Pseudomonas aeruginosa strains PAO1 and PA14, which exhibit similar exponential trends of surface cell population increase, show unanticipated differences when the behavior of each cell was considered at the full lineage level and interpreted using the unifying quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two complementary surface colonization strategies, which are roughly analogous to “immediate-” vs “deferred-gratification” in a prototypical cognitive-affective processing system. PAO1 lineages commit relatively quickly to a surface compared to PA14 lineages. PA14 lineages allow detaching cells to retain memory of the surface so that they are primed for improved subsequent surface attachment. In fact, it is possible to identify motility suppression events in PA14 lineages in the process of surface commitment. We hypothesize that these contrasting strategies are rooted in downstream differences between Wsp-based and Pil-Chp-based surface sensing systems.

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.