Nearby boundaries create eddies near microscopic filter feeders

178

167

The exchange of nutrients and dissolved gasses between corals and their environment is a critical determinant of the growth of coral colonies and the productivity of coral reefs. To date, this exchange has been assumed to be limited by molecular diffusion through an unstirred boundary layer extending 1-2 mm from the coral surface, with corals relying solely on external flow to overcome this limitation. Here, we present direct microscopic evidence that, instead, corals can actively enhance mass transport through strong vortical flows driven by motile epidermal cilia covering their entire surface. Ciliary beating produces quasi-steady arrays of counterrotating vortices that vigorously stir a layer of water extending up to 2 mm from the coral surface. We show that, under low ambient flow velocities, these vortices, rather than molecular diffusion, control the exchange of nutrients and oxygen between the coral and its environment, enhancing mass transfer rates by up to 400%. This ability of corals to stir their boundary layer changes the way that we perceive the microenvironment of coral surfaces, revealing an active mechanism complementing the passive enhancement of transport by ambient flow. These findings extend our understanding of mass transport processes in reef corals and may shed new light on the evolutionary success of corals and coral reefs.coral microenvironment | coral reef evolution | diffusion boundary layer | microfluidics | biological fluid mechanics

Section: Significancementioning

confidence: 94%

Vortical ciliary flows actively enhance mass transport in reef corals

Shapiro

Fernández

Garren

et al. 2014

178

167

“…These observations raise the question of whether the mantle-driven flow could play a direct role in delivering suspended particles to the ciliated surface. Such particle capture from oncoming flow has been rigorously studied in aquatic suspension filter feeders (21)(22)(23)(24). Mechanisms for particle capture include direct interception, inertial impaction, gravitational deposition, diffusion, and motile-particle deposition (5).…”

Section: Resultsmentioning

confidence: 99%

Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome

Nawroth

Guo

Koch

et al. 2017

109

103

We show that mucociliary membranes of animal epithelia can create fluid-mechanical microenvironments for the active recruitment of the specific microbiome of the host. In terrestrial vertebrates, these tissues are typically colonized by complex consortia and are inaccessible to observation. Such tissues can be directly examined in aquatic animals, providing valuable opportunities for the analysis of mucociliary activity in relation to bacteria recruitment. Using the squid-vibrio model system, we provide a characterization of the initial engagement of microbial symbionts along ciliated tissues. Specifically, we developed an empirical and theoretical framework to conduct a census of ciliated cell types, create structural maps, and resolve the spatiotemporal flow dynamics. Our multiscale analyses revealed two distinct, highly organized populations of cilia on the host tissues. An array of long cilia (∼25 µm) with metachronal beat creates a flow that focuses bacteria-sized particles, at the exclusion of larger particles, into sheltered zones; there, a field of randomly beating short cilia (∼10 µm) mixes the local fluid environment, which contains host biochemical signals known to prime symbionts for colonization. This cilia-mediated process represents a previously unrecognized mechanism for symbiont recruitment. Each mucociliary surface that recruits a microbiome such as the case described here is likely to have system-specific features. However, all mucociliary surfaces are subject to the same physical and biological constraints that are imposed by the fluid environment and the evolutionary conserved structure of cilia. As such, our study promises to provide insight into universal mechanisms that drive the recruitment of symbiotic partners.cilia | microfluidics | host-bacterial symbiosis | biological fluid mechanics, biofiltration M any eukaryotic cells feature motile cilia, microtubulebased surface actuators that sense and propel the extracellular fluidic environment (1-3). Whereas cilia and cilia-like structures that sort and capture bacteria or particles are common and well-characterized features of aquatic organisms (4-7), in terrestrial animals such as mammals, the internal location of ciliated surfaces has made them difficult to study. A central challenge in internal ciliated mucus membranes, such as those lining the fallopian tube, the Eustachian tube, and the respiratory system (8), is to reconcile the effective clearance of toxic molecules and undesirable microbes with selective engagement of beneficial symbionts. For example, on airway epithelia, the coordinated beat of motile cilia creates a horizontal flow across their tips (9-12), which clears mucus, microorganisms, and debris (Fig. 1A). Disruption of this mucociliary clearance can lead to chronic infection of the airways (13). However, this simple model is incomplete; ciliated airway epithelia not only serve a clearance function, but also provide a habitat and a gateway for coevolved symbionts that play an essential role in the development of the host...

“…At these transitional values, diffusion is still a dominant mode of transport but advection also becomes significant and the generation of feeding currents can theoretically enhance nutrient uptake. Previous studies have investigated the generation of feeding currents using model swimmers with simplified geometries (5,7,20), and prescribed deformations (21,22). Here we consider instead general stroke patterns for our model biflagellate and address questions related to the adaptation, efficiency, and existence of optimal swimming gaits with respect to nutrient uptake.…”

Section: A-dmentioning

confidence: 99%

Optimal feeding and swimming gaits of biflagellated organisms

Tam

Hosoi

2011

Locomotion is widely observed in life at micrometric scales and is exhibited by many eukaryotic unicellular organisms. Motility of such organisms can be achieved through periodic deformations of a tail-like projection called the eukaryotic flagellum. Although the mechanism allowing the flagellum to deform is largely understood, questions related to the functional significance of the observed beating patterns remain unresolved. Here, we focus our attention on the stroke patterns of biflagellated phytoplanktons resembling the green alga Chlamydomonas. Such organisms have been widely observed to beat their flagella in two different ways-a breaststroke and an undulatory stroke-both of which are prototypical of general beating patterns observed in eukaryotes. We develop a general optimization procedure to determine the existence of optimal swimming gaits and investigate their functional significance with respect to locomotion and nutrient uptake. Both the undulatory and the breaststroke represent local optima for efficient swimming. With respect to the generation of feeding currents, we found the breaststroke to be optimal and to enhance nutrient uptake significantly, particularly when the organism is immersed in a gradient of nutrients.optimization | stroke kinematics | low Reynolds number | efficiency T he vast majority of living organisms are found in an astonishing diversity at micrometric scales. Such seemingly simple unicellular organisms interact with their surroundings and exhibit complex dynamic behaviors in order to access resource-rich environments. The ability to locate and take advantage of such favorable environments relies on a rapid chemotactic response (1, 2). In this paper, we investigate the motility of specific microorganisms to address questions related to the functional adaptation, efficiency, and optimization of biolocomotion.A dominant trait shared by many microorganisms is the prevalence of flagella as motility appendages. The structure of the axoneme, which constitutes the core of the eukaryotic flagellum, is extremely well preserved across the eukaryotic domain. This same structure is found to propel sperm cells and, when several of them beat collectively as cilia, to expel mucus from human lungs. The eukaryotic flagellum has a complex internal "9 þ 2" microtubule structure (3), whose elaborate molecular machinery allows the flagellum to induce local bending moments and actively deform its shape. It is noteworthy that these flagella are widely observed to beat in two significantly different ways: undulatory traveling waves that propagate down the flagellum (as exhibited by sperm cells), and so-called "effective recovery" strokes commonly observed in cilia. Because it is possible for organisms to alter and control the waveform along the flagellum, it is of interest to investigate the functional significance of these specific flagellar stroke patterns and their utility with respect to swimming and feeding.Previous investigations of nutrient transport and hydrodynamics around microorganisms (4...