Sperm chemotaxis in marine species is optimal at physiological flow rates according theory of filament surfing

Sperm of marine invertebrates have to find eggs cells in the ocean. Turbulent flows mix sperm and egg cells up to the millimeter scale; below this, active swimming and chemotaxis become important. Previous work addressed either turbulent mixing or chemotaxis in still water. Here, we present a general theory of sperm chemotaxis inside the smallest eddies of turbulent flow, where signaling molecules released by egg cells are spread into thin concentration filaments. Sperm cells 'surf' along these filaments towards the egg. External flows make filaments longer, but also thinner. These opposing effects set an optimal flow strength. The optimum predicted by our theory matches flow measurements in shallow coastal waters. Our theory quantitatively agrees with two previous fertilization experiments in Taylor-Couette chambers and provides a mechanistic understanding of these early experiments. 'Surfing along concentration filaments' could be a paradigm for navigation in complex environments in the presence of turbulent flow. Author summary Many motile cells navigate in complex environments along concentration gradients of signaling molecules. This chemotaxis has been studied extensively both experimentally and theoretically, yet mostly for idealized conditions of perfect chemical gradients. But under physiological conditions, concentration fields are subject to distortions, e.g., by turbulent flows in the ocean. Pioneering experiments suggest that in species with external fertilization, chemotaxis of sperm cells towards the egg may even work better at an optimal flow strength compared to conditions of still water. Yet to date, the mechanistic cause for this optimum is not known. We present a general theory of chemotactic navigation in external flow. We characterize how external flow distorts concentration fields into long filaments, and show how chemotaxing cells can subsequently 'surf' along these filaments towards a chemoattractant source. Stronger flows make concentration filaments longer, but also thinner; together, these two counter-acting effects set an optimal flow strength. Beyond fertilization of marine invertebrates, we believe that 'surfing along concentration filaments' could be a more general paradigm, relevant also for the ecology of marine bacteria feeding on organic marine snow in the ocean, or chemotaxis inside multi-cellular organisms with internal flows.

Automated summary

Marine invertebrate sperm need to find egg cells in the ocean through turbulent mixing and cellular chemotaxis. External flows elongate concentration filaments of signaling molecules, along which sperm cells 'surf' towards the eggs. The theory of chemotactic navigation in external flow provides insights into how cells navigate in complex environments under turbulent conditions.