Odd dynamics in living chiral crystals

Living matter exhibits complex non-equilibrium behavior. Here, we report on the formation of chiral crystals of starfish embryos which undergo autonomous order-disorder transitions. Embryos form a stable bound state at the water-air interface and hydrodynamically self-assemble into 2D crystals with hexagonal order. As a function of developmental time, these 2D crystals undergo an order-disorder transition characterized by progressive loss of translational and orientational order. Remarkably, non-reciprocal force and torque exchanges between embryos lead to emergence of chiral waves and odd-elastic mechanical response. Our hydrodynamic model elucidates how near field interactions can lead to the experimentally observed emergent dynamics.

Related publication: Tan TH*, Mietke A*, Li J, Chen Y, Higinbotham H, Gokhale S, Foster PJ, Dunkel J, Fakhri N. “Odd dynamics of living chiral crystals.Nature (2022), 607(7918), 287-293.

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Emergent chirality in active solid rotation of pancreas spheres

Collective cell dynamics play a crucial role in many developmental and physiological contexts. In this work, we use murine pancreas-derived organoids to study tissue rotation, a phenomenon widely reported both in vivo and in vitro. Using a 3D vertex model, we demonstrate how the interplay between traction force and polarity alignment can account for these distinct rotational dynamics. Furthermore, our analysis shows that the spherical tissue rotates as an active solid and exhibits spontaneous chiral symmetry breaking. Using a continuum model, we demonstrate how the types and location of topological defects in the polarity field underlie this symmetry breaking process. Altogether, our work shows that tissue chirality can arise via topological defects in the pattern of cell traction forces, with potential implications for left-right symmetry breaking processes in morphogenetic events.

Related publication: Tan TH*, Amiri A*, Barandiaran IS*, Staddon M, Hermann A, Tomas S, Duclut C, Papovic M, Julicher F, Grapin-Botton A. “Emergent chirality in active solid rotation of pancreas spheres.Submitted 2022.

Decoding cell shape information using protein patterns

Many cellular and developmental processes rely on the precise positioning of proteins to ensure proper morphogenesis. Such protein patterns are susceptible to cell and tissue shape changes, raising the question of how these patterns can be robust in a mechanically dynamic environment. In this project, we elucidate a mechanism that pattern protein localization robustly despite cell shape deformations. By combining quantitative experiments in starfish oocytes with mathematical modelling, we find that cell shape information encoded in a cytosolic gradient can be decoded by a bistable front of a RhoA regulator. In turn, this bistable front precisely positions RhoA by locally triggering excitable dynamics. We posit that this hierarchical coupling between a biochemical gradient and protein self-organization provides mechanochemical feedback for cell shape sensing and control in early oocyte and embryo development.

Related publication: Wigbers M*, Tan TH*, Brauns F, Jinghui L, Swartz Z, Frey E, Fakhri N (2021) “A hierarchy of protein patterns robustly decodes cell shape information.Nature Physics.

Tuning mechanical structures in cells via state transition

The actomyosin cortex, consisting of filamentous actin, myosin molecular motors and various cross-linking proteins, is a thin layer of structure beneath the cell membrane that regulates cell shape. To understand how this multi-component system gives rise to emergent mechanical properties, we used a reconstituted system to study how cross-linker protein concentration modulates the structure and dynamics of actomyosin cortex. We discovered that as the amount of cross-linking is tuned, the system transitions from a free-flowing state with maximal susceptibility to a contractile state, suggesting that cross-linker concentration could be used to induce major structural reorganization in the actomyosin cortex and dynamically regulate cell mechanics.

Related publication: Tan TH*, Malik-Garbi M*, Abu-Shah E*, Li J, Sharma A, MacKintosh FC, Keren K, Schmidt CF and Fakhri N, (2018) “Self-organized stress patterns drive state transitions in actin cortices.Science Advances, 4(6), p.eaar2847.

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Turbulent dynamics in membrane signaling

Starfish oocyte membrane exhibits Rho spiral wave dynamics when the GEF protein is over-expressed. Using phase and topological analysis, we showed that the membrane Rho spiral wave dynamics can be understood as interactions between topological defects in the phase field. These tools could be extended to the study of excitable spiral dynamics in neuronal systems and cardiac arrhythmia. Recent studies have also revealed the importance of topological defects in collective multicellular behaviors, implying that topological aspects of biological systems could have functional importance.

Related publication: Tan TH*, Liu J*, Miller PW*, Tekant M, Dunkel J, and Fakhri N, (2020) “Topological turbulence in the membrane of a living cell.Nature Physics. [PDF]

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Probing cellular energetics via irreversibility

Cellular structures constantly consume and dissipate energy on a variety of spatiotemporal scales in order to function. Their inherent multi-scale nature makes it challenging to unravel the mechanisms underlying the observed nonequilibrium activity. By analyzing probe particles embedded in the starfish oocyte cortex and using a multi-scale irreversibility metric, we extract model-independent estimates of the time-scales of energy dissipation. We further demonstrate that the irreversibility measure maintains a monotonic relationship with the underlying biological nonequilibrium activity. More generally, this irreversibility metric can be used to identify activity time scales in various biological systems.

Related publication: Tan TH*, Watson GA*, Chao YC*, Gingrich TR, Horowitz JM, and Fakhri N “Scale-dependent irreversibility in living matter.Submitted.

"Run-and-tumble" in plant roots

Plant roots exhibit nontrivial architecture to optimize absorption of nutrients and water. During my undergraduate in the Cohen lab, I studied the role of mechanics in plant root gravitropism. By imaging the Medicago truncatula primary root morphology growing on different tilt angles and applying tools from statistical mechanics, I showed that plant roots navigate their environment using a strategy similar to that used by the bacteria E. Coli. Essentially, the plants switch their growth direction more frequently and towards the downhill direction at a rate proportional to the angle between the root tip and the direction of gravity. This ‘grow-and-switch’ mechanism explains the different root patterns such as coiling and waving. These results suggest a method for controlling root architecture to enhance agricultural crop yields. More generally, these results speak to the subtle interplay between root biology and mechanics that produces the amazing morphologies roots create as they grow.

Related publication: Tan TH, Silverberg JL, Floss DS, Harrison MJ, Henley CL and Cohen I, (2015) “How grow-and-switch gravitropism generates root coiling and root waving growth responses in Medicago truncatula.Proceedings of the National Academy of Sciences, 112(42), pp.12938-12943. | See also research highlight in Nature Physics 11 (2015) and Cornell Chronicle report.