Entangled architecture of rough endoplasmic reticulum (RER) and vacuoles enables topological damping in cytoplasm of an ultra-fast giant cell

Abstract

Cellular systems are known to exhibit some of the fastest movements in biology - but little is known as to how single cells can dissipate this energy rapidly and adapt to such large accelerations without disrupting internal architecture. To address this, we investigate Spirostomum ambiguum - a giant cell (1-4 mm in length) well-known to exhibit ultrafast contractions (50% of body length) within 5 msec with a peak acceleration of 15g. Utilizing transmitted electron microscopy (TEM) and confocal imaging, we discover a novel association of rough endoplasmic reticulum (RER) and vacuoles throughout the cell - forming a contiguous fenestrated membrane architecture that topologically entangles these two organelles. A nearly uniform inter-organelle spacing of 60 nm is observed between RER and vacuoles, closely packing the entire cell. Inspired by the entangled organelle structure, we study the mechanical properties of entangled deformable particles using a vertex-based model, with all simulation parameters matching 10 dimensionless numbers to ensure dynamic similarity. We demonstrate how entangled deformable particles respond to external loads by an increased viscosity against squeezing and help preserve spatial relationships. Because this enhanced damping arises from the entanglement of two networks incurring a strain-induced jamming transition at subcritical volume fractions, which is demonstrated through the spatial correlation of velocity direction, we term this phenomenon "topological damping". Our findings suggest a new mechanical role of RER-vacuolar meshwork as a metamaterial capable of damping an ultra-fast contraction event. Significance StatementLittle is known about how single-cell organisms with extreme motility can decelerate or dissipate energy, as they lack connective tissues. Our study discovered a novel entangled rough endoplasmic reticulum (RER)-vacuolar meshwork architecture in Spirostomum ambiguum, an ultrafast giant cell that can contract itself with 15g accelerations. We demonstrate through an entangled deformable particle model that the entangled architecture increases the squeeze-flow viscosity of particle systems and helps dampen the motion, a phenomenon we called "topological damping". For biologists, our study suggests the mechanical role of RER through topological constraints on nearby organelles. For physicists, we point out a new way to create a system with strain-induced jamming. For engineers, we present a novel architecture that can provide braking functions.