Effects of prey capture on the swimming and feeding performance of choanoflagellates

Abstract

Locomoting organisms often carry loads such as captured prey or young. Load-carrying effects on high-Reynolds-number flight have been studied, but the fluid dynamics of load carrying by low-Reynolds-number microorganisms has not. We studied low-Reynolds-number load carrying using unicellular choanoflagellates, which wave a flagellum to swim and create a water current transporting bacterial prey to a food-capturing collar of microvilli. A regularized Stokeslet framework was used to model the hydrodynamics of a swimming choanoflagellate with bacterial prey on its collar. Both the model and microvideography of choanoflagellates showed that swimming speed decreases as number of prey being carried increases. Flux of water into the capture zone is reduced by bacteria on the collar, which redirect the water flow and occlude parts of the collar. Feeding efficiency (prey captured per work to produce the feeding current) is decreased more by large prey, prey in the plane of flagellar beating and prey near microvillar tips than by prey in other locations. Some choanoflagellates can attach themselves to surfaces. We found that the reduction in flux due to bacterial prey on the collars of these attached thecate cells was similar to the reduction in flux for swimmers.

Electrical signaling and coordinated behavior in the closest relative of animals

“…Though we find instances of phagocytic cups forming during strong calcium transients ( Figure S12 ), the primary response appears to consist of the arrest of the flagella, contraction along the apical-basal axis, and shedding of bacteria from the feeding collar. Modeling of choanoflagellate filter feeding suggests that the bacterial load on the collar strongly affects the ability of the flagella to generate flow as well as the cells’ ability to propel itself forward[45,46]. It is possible that the here described behavior functions to balance feeding efficiency with the ability to disperse or simply maintain a high level of flow through the collar region.…”