Oscillatory fluid flow drives scaling of contraction wave with system size

Abstract

Flows over remarkably long distances are crucial to the functioning of many organisms, across all kingdoms of life. Coordinated flows are fundamental to power deformations, required for migration or development, or to spread resources and signals. A ubiquitous mechanism to generate flows, particularly prominent in animals and amoeba, is acto-myosin cortex driven mechanical deformations that pump the fluid enclosed by the cortex. Yet, it is unclear how cortex dynamics can self-organize to give rise to coordinated flows across the largely varying scales of biological systems. Here, we develop a mechanochemical model of acto-myosin cortex mechanics coupled to a contraction-triggering, soluble chemical. The chemical itself is advected with the flows generated by the cortex driven deformations of the tubular-shaped cell. The theoretical model predicts a dynamic instability giving rise to stable patterns of cortex contraction waves and oscillatory flows. Surprisingly, simulated patterns extend beyond the intrinsic length scale of the dynamic instability -scaling with system size instead. Patterns appear randomly but can be robustly generated in a growing system or by flow-generating boundary conditions. We identify oscillatory flows as the key for the scaling of contraction waves with system size. Our work shows the importance of active flows in biophysical models of patterning, not only as a regulating input or an emergent output, but rather as a full part of a self-organized machinery. Contractions and fluid flows are observed in all kinds of organisms, so this concept is likely to be relevant for a broad class of systems.

Living System Adapts Harmonics of Peristaltic Wave for Cost-Efficient Optimization of Pumping Performance

“…Living systems, as exemplified here, use the phase difference between harmonics as a key cost efficient parameter to adjust wave performance. Specifically, control may reside in the inherent nonlinear material properties that may change upon environmental stimuli [44]. It is inspiring to speculate that life's biochemical machinery can quickly adjust its viscoelastic properties of an actin cortex, e.g., by controlling the access to globular actin via secondary proteins [45].…”

The Shape and Function of Solid Fascias Depend on the Presence of Liquid Fascias

“…The cell is full of cytoplasm, as well as the membrane that surrounds it is rich in fluids; externally we find the extracellular matrix with interstitial fluids and more consistent hydrostatic pressure changes due to the presence of vessels containing lymph and blood [3]. Without the fluids, the deformation of the cell would not occur, there would be no movement of the actomyosin complex, there would be no transport of biochemical or electrical activity [25]. The movement of cellular fluids occurs with self-regulating patterns (rhythmic waves); the waves produced not only carry the signals produced at distances and at higher speeds than the protein connections between the extracellular matrix and the nucleus, but the wave itself represents an electro-mechanicalchemical signal [25].…”

“…Mechanotransduction is a fundamental mechanism for the adaptation of the human body, where, a mechanical stimulus alters the shape of the cell, which responds with an electrochemical cascade [24]. The classic chemical-mechanical model looks at calcium as the initiator of the contraction of the actomyosin complex, which complex is capable of deforming the cell [25]. The contraction is used to understand the surrounding mechanometabolic environment and to get the mechanical information to the nucleus of the cell; moreover, this deformation is felt by other cells [25].…”

“…The classic chemical-mechanical model looks at calcium as the initiator of the contraction of the actomyosin complex, which complex is capable of deforming the cell [25]. The contraction is used to understand the surrounding mechanometabolic environment and to get the mechanical information to the nucleus of the cell; moreover, this deformation is felt by other cells [25]. The mechanical deformation of the cell is not only an adaptation but a means of communication [3].…”

“…Without the fluids, the deformation of the cell would not occur, there would be no movement of the actomyosin complex, there would be no transport of biochemical or electrical activity [25]. The movement of cellular fluids occurs with self-regulating patterns (rhythmic waves); the waves produced not only carry the signals produced at distances and at higher speeds than the protein connections between the extracellular matrix and the nucleus, but the wave itself represents an electro-mechanicalchemical signal [25]. Unfortunately, we still lack many more detailed elements to understand this mechanism, but there is no doubt that this fluidic phenomenon is of primary importance.…”