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Choanoflagellates are unicellular eukaryotes that are ubiquitous in aquatic habitats. They have a single flagellum that creates a flow toward a collar filter composed of filter strands that extend from the cell. In one common group, the loricate choanoflagellates, the cell is suspended in an elaborate basket-like structure, the lorica, the function of which remains unknown. Here, we use Computational Fluid Dynamics to explore the possible hydrodynamic function of the lorica. We use the choanoflagellate Diaphaoneca grandis as a model organism. It has been hypothesized that the function of the lorica is to prevent refiltration (flow recirculation) and to increase the drag and, hence, increase the feeding rate and reduce the swimming speed. We find no support for these hypotheses. On the contrary, motile prey are encountered at a much lower rate by the loricate organism. The presence of the lorica does not affect the average swimming speed, but it suppresses the lateral motion and rotation of the cell. Without the lorica, the cell jiggles from side to side while swimming. The unsteady flow generated by the beating flagellum causes reversed flow through the collar filter that may wash away captured prey while it is being transported to the cell body for engulfment. The lorica substantially decreases such flow, hence it potentially increases the capture efficiency. This may be the main adaptive value of the lorica.

Leuconoid sponges are filter-feeders with a complex system of branching inhalant and exhalant canals leading to and from the close-packed choanocyte chambers. Each of these choanocyte chambers holds many choanocytes that act as pumping units delivering the relatively high pressure rise needed to overcome the system pressure losses in canals and constrictions. Here, we test the hypothesis that, in order to deliver the high pressures observed, each choanocyte operates as a leaky, positive displacement-type pump owing to the interaction between its beating flagellar vane and the collar, open at the base for inflow but sealed above. The leaking backflow is caused by small gaps between the vaned flagellum and the collar. The choanocyte pumps act in parallel, each delivering the same high pressure, because low-pressure and high-pressure zones in the choanocyte chamber are separated by a seal (secondary reticulum). A simple analytical model is derived for the pump characteristic, and by imposing an estimated system characteristic we obtain the back-pressure characteristic that shows good agreement with available experimental data. Computational fluid dynamics is used to verify a simple model for the dependence of leak flow through gaps in a conceptual collar-vane-flagellum system and then applied to models of a choanocyte tailored to the parameters of the freshwater demosponge Spongilla lacustris to study its flows in detail. It is found that both the impermeable glycocalyx mesh covering the upper part of the collar and the secondary reticulum are indispensable features for the choanocyte pump to deliver the observed high pressures. Finally, the mechanical pump power expended by the beating flagellum is compared with the useful (reversible) pumping power received by the water flow to arrive at a typical mechanical pump efficiency of about 70%.

Microbial filter feeders are an important group of grazers, significant to the microbial loop, aquatic food webs, and biogeochemical cycling. Our understanding of microbial filter feeding is poor, and, importantly, it is unknown what force microbial filter feeders must generate to process adequate amounts of water. Also, the trade-off in the filter spacing remains unexplored, despite its simple formulation: A filter too coarse will allow suitably sized prey to pass unintercepted, whereas a filter too fine will cause strong flow resistance. We quantify the feeding flow of the filter-feeding choanoflagellate Diaphanoeca grandis using particle tracking, and demonstrate that the current understanding of microbial filter feeding is inconsistent with computational fluid dynamics (CFD) and analytical estimates. Both approaches underestimate observed filtration rates by more than an order of magnitude; the beating flagellum is simply unable to draw enough water through the fine filter. We find similar discrepancies for other choanoflagellate species, highlighting an apparent paradox. Our observations motivate us to suggest a radically different filtration mechanism that requires a flagellar vane (sheet), something notoriously difficult to visualize but sporadically observed in the related choanocytes (sponges). A CFD model with a flagellar vane correctly predicts the filtration rate of D. grandis , and using a simple model we can account for the filtration rates of other microbial filter feeders. We finally predict how optimum filter mesh size increases with cell size in microbial filter feeders, a prediction that accords very well with observations. We expect our results to be of significance for small-scale biophysics and trait-based ecological modeling., Competing Interests: The authors declare no conflict of interest.