A hydraulic instability drives the cell death decision in the nematode germline

Abstract

Oocytes are large cells that develop into an embryo upon fertilization1. As interconnected germ cells mature into oocytes, some of them grow—typically at the expense of others that undergo cell death2–4. We present evidence that in the nematode Caenorhabditis elegans, this cell-fate decision is mechanical and related to tissue hydraulics. An analysis of germ cell volumes and material fluxes identifies a hydraulic instability that amplifies volume differences and causes some germ cells to grow and others to shrink, a phenomenon that is related to the two-balloon instability5. Shrinking germ cells are extruded and they die, as we demonstrate by artificially reducing germ cell volumes via thermoviscous pumping6. Our work reveals a hydraulic symmetry-breaking transition central to the decision between life and death in the nematode germline.

A hydro-osmotic coarsening theory of biological cavity formation

“…In spite of these simplifications, we have shown importantly that active ion pumping can bias coarsening spatially. Active osmotic volume control emerges hence as a novel mode of symmetry breaking for tissue morphogenesis, that could be relevant also to oogenesis [36,39,40], to liquid phase transition of biological condensates [68] and to plant tissue growth [42,44]. This symmetry breaking may complement or compete with mechanical gradients, that were shown to play a major role in mouse embryo blastocoel formation [18] or in the coarsening of membrane-less organelles [69,70].…”

“…Hydraulic and osmotic flows are indeed more and more recognized as essential determinants of embryo and tissue shaping [18,[35][36][37][38][39][40]. However only a few physical models describe the interplay between cell mechanics, osmotic effects and fluid flow in morphogenesis [41][42][43][44], and in all those previous models, osmolarity is considered July 15, 2021 2/21 spatially homogeneous.…”

“…Here, we propose a generic physical model to describe the hydro-osmotic coupling between pressurized compartments, explicitly accounting for osmotic gradients and ion pumping. Our model may therefore also form a relevant theoretical framework to describe the coupled dynamics between nurse cells and the future oocyte during Drosophila oogenesis [36,39], or between germ cells in the nematode C elegans [40]. Here, we do not study however the initial nucleation of small cavities.…”

A hydro-osmotic coarsening theory of biological cavity formation

“…Hydraulic and osmotic flows are indeed more and more recognized as essential determinants of embryo and tissue shaping [19,[36][37][38][39][40][41]. However only a few physical models describe the interplay between cell mechanics, osmotic effects and fluid flow in morphogenesis [42][43][44][45], and in all those previous models, osmolarity is considered spatially homogeneous.…”

“…Here, we propose a generic physical model to describe the hydro-osmotic coupling between pressurized compartments, explicitly accounting for osmotic gradients and ion pumping. Our model may therefore also form a relevant theoretical framework to describe the coupled dynamics between nurse cells and the future oocyte during Drosophila oogenesis [37,40], or between germ cells in the nematode C elegans [41]. Here, we do not study however the initial nucleation of small cavities.…”