Hydrodynamics of microbial filter feeding

Abstract

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. protozoans | choanoflagellates | filter feeding | microswimmers | computational fluid dynamics H eterotrophic microorganisms in the oceans inhabit a dilute environment and they need efficient feeding mechanisms to acquire enough food to sustain growth (1, 2). At the microscale the Reynolds number is low and viscous forces govern hydrodynamical interactions. This implies extensive, long-range flow disturbances around moving particles and microswimmers, impeding cell-cell contact and prey capture (3, 4). However, to encounter enough food, purely heterotrophic plankton that rely solely on prey capture typically need to clear a volume of water for prey corresponding to 1 million times their own body volume per day (4). Thus, heterotrophic microbes face a difficult challenge, and the prevailing viscous forces must strongly influence prey capture and shape the various feeding modes through evolution.Many unicellular flagellates as well as colonial sponges and metazoans, e.g., tunicates, use filter feeding to catch bacteriasized prey (1, 5-7). They establish a feeding current, from which prey particles are sieved using filter structures. Such filter feeders benefit from having filters with small mesh size that allow the organisms to capture small prey (5, 8). However, filter ...

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates

“…The swimming speeds we calculated for slow and fast swimmers ( figure 3) fall within the For the flagellar kinematics of a typical S. rosetta choanoflagellate, we calculated the inward flux during one beat cycle to be approximately 19.01 mm 3 for a slow swimmer and 15.76 mm 3 for a thecate cell tethered mid-water, which produces clearance rates (volume flow rate through the capture zone) of 461.84 mm 3 s 21 and 383.01 mm 3 s 21 , respectively, at the beat frequency of 24.3 Hz. These are at the low end of clearance rates reported for other species of choanoflagellates by Nielsen et al [25], some directly measured and some estimated using published experimental data, between 400 mm 3 s 21 and 4400 mm 3 s 21 .…”

“…Their model included a representation of the cell body, the collar of microvilli and the undulatory flagellum. Their results suggested that a thin cylindrical flagellum could not account for experimentally measured water fluxes, and they proposed that the flagellum of this species has a broad vane [25]. Another earlier computational study of choanoflagellate hydrodynamics, using a regularized Stokeslet framework, modelled the effect on the flow of a lorica, a basket-like structure that is not present in the S. rosetta cells considered here [26].…”

“…As described above, we calculated the volume flow rate through the capture zone (clearance rate) of a slow swimmer and of a thecate S. rosetta to be 461.84 mm 3 s 21 and 383.01 mm 3 s 21 , respectively. Nielsen et al [25] calculated the clearance rate for Diaphanoeca grandis, a choanoflagellate whose cell body and collar are surrounded by a lorica that forces the water pumped by the flagellum to move through the collar. In their CFD model, they held the cell stationary, thereby not including the contributions to inward flux of the swimming and the periodic rocking motion of the cell, which we found to be important for slow swimmers.…”

Nutrient Transport Driven by Microbial Active Carpets

“…One of the most beautiful examples, which also highlights the importance of multicellular cooperation, is the rosette structure in many species of choanoflagellates [96]. These free-living cell groups generate dipolar flows [97,98] when not sessile and also accumulate as carpets on surfaces [99], acting like aggregate random walkers [100]. To our knowledge, the idea that accrued groups of such organisms could optimise the attraction of nutrients collectively has not been explored much in the current literature.…”

A novel mechanism of mixing by pulsing corals

“…Organisms that increase in size may extend ( partly) out of the boundary layer, ensuring that at least part of their surface is exposed to regions of high mixing. Behavioral adaptations to life in the boundary layer include the generation of jets (Santhanakrishnan et al, 2012), the use of cilia or flagella to create local flows (Petersen, 2007;Nielsen et al, 2017), or any other behavior resulting in increased fluid mixing and thus local reduction in boundary layer thickness.…”