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

Abstract

AbstractCellular systems are known to exhibit some of the fastest movements in the biological world 1–3 - but little is known as to how single cells can dissipate this energy rapidly and adapt to such large accelerations without sub-cellular damage. To study intracellular adaptations under extreme forces - we investigate Spirostomum ambiguum - a giant cell (1-4mm in length) well known to exhibit ultrafast contractions (50% of body length) within 5 msec with a peak acceleration of 15g. 2,4 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 cubic membrane architecture that topologically entangles these two organelles. A nearly uniform inter-organelle spacing of 60nm is observed between RER and vacuoles, closely packing the entire cell. Using an overdamped molecular dynamics simulation, 5 we demonstrate how this unique entangled metamaterial responds to external loads by rapidly dissipating energy and helps preserve spatial relationships between organelles. Because this dynamics arises primarily from entanglement of two networks incurring jamming transition at a subcritical volume fraction 6 - we term this phenomena ”topological damping”. Our findings suggest a new mechanical role of RER-vacuolar meshwork as a metamaterial capable of dissipating energy in an ultra-fast contraction event.