Fluid Dynamics of Multiple Fast-Firing Extrusomes : Fast extrusomes.

Abstract

The contact and puncturing of cells and organisms in fluid at microscales are difficult due to viscous-dominated effects and the interactions of boundary layers. This challenge can be overcome in part through the ultra-fast firing of organelles such as the nematocysts of jellyfish. Such super-fast extrusive organelles found in cnidarians, protists, and dinoflagellates are known as extrusomes. It has previously been shown that a single barb at the cellular microscale must be fired fast enough to reach the inertial regime to contact prey. The fluid physics of multiple-fired extrusomes has not been carefully studied, however. The simultaneous firing of extrusomes can be seen in nature, with one example being the dinoflagellate Nematodunium, where each nematocyst consists of a ring of parallel sub-capsules similar to a Gatling gun. In this paper, the immersed boundary method was used to numerically simulate the dynamics of one, two, and three barb-like structures that are accelerated and released towards a passive elastic prey in two dimensions. We considered the simultaneous release of all three barbs as well as a sequential release of the barbs. We also vary the Reynolds number of the simulation for several orders of magnitude to consider the biologically relevant range of extrusome firing, given that different organelles are fired at different speeds and that some extrusomes are fired in viscous mucus. For multiple barbs, we found that there is a nonmonotonic relationship between the distance between the top of the center barb and the prey and the Reynolds number when fired simultaneously. This is because the prey is not pushed out of the way by boundary effects at higher Reynolds numbers, while barbs at lower Reynolds numbers entrain more fluid and are carried farther. Furthermore, the center barbs at the highest Reynolds numbers always hit the prey and are robust to firing order and the spacing between barbs. Overall, our simple model shows that the extreme nonlinearity of the fluid at this scale results in nonmonotonic relationships between the distance to the prey and various parameters.