An official website of the United States government
Abstract Choanoflagellates, unicellular eukaryotes that can form multicellular colonies by cell division and that share a common ancestor with animals, are used as a model system to study functional consequences of being unicellular versus colonial. This review examines performance differences between unicellular and multicellular choanoflagellates in swimming, feeding, and avoiding predation, to provide insights about possible selective advantages of being multicellular for the protozoan ancestors of animals. Each choanoflagellate cell propels water by beating a single flagellum and captures bacterial prey on a collar of microvilli around the flagellum. Formation of multicellular colonies does not improve the swimming performance, but the flux of prey‐bearing water to the collars of some of the cells in colonies of certain configurations can be greater than for single cells. Colony geometry appears to affect whether cells in colonies catch more prey per cell per time than do unicellular choanoflagellates. Although multicellular choanoflagellates show chemokinetic behavior in response to oxygen, only the unicellular dispersal stage (fast swimmers without collars) use pH signals to aggregate in locations where bacterial prey might be abundant. Colonies produce larger hydrodynamic signals than do single cells, and raptorial protozoan predators capture colonies while ignoring single cells. In contrast, ciliate predators entrain both single cells and colonies in their feeding currents, but reject larger colonies, whereas passive heliozoan predators show no preference. Thus, the ability of choanoflagellate cells to differentiate into different morphotypes, including multicellular forms, in response to variable aquatic environments might have provided a selective advantage to the ancestors of animals.
more »
« less
Effects of prey capture on the swimming and feeding performance of choanoflagellates
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.
more »
« less
- Award ID(s):
- 2054143
- PAR ID:
- 10549837
- Publisher / Repository:
- Flow
- Date Published:
- Journal Name:
- Flow
- Volume:
- 3
- ISSN:
- 2633-4259
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Microbial eukaryotes, critical links in aquatic food webs, are unicellular, but some, such as choanoflagellates, form multicellular colonies. Are there consequences to predator avoidance of being unicellular vs. forming larger colonies? Choanoflagellates share a common ancestor with animals and are used as model organisms to study the evolution of multicellularity. Escape in size from protozoan predators is suggested as a selective factor favoring evolution of multicellularity. Heterotrophic protozoans are categorized as suspension feeders, motile raptors, or passive predators that eat swimming prey which bump into them. We focused on passive predation and measured the mechanisms responsible for the susceptibility of unicellular vs. multicellular choanoflagellates,Salpingoeca helianthica, to capture by passive heliozoan predators,Actinosphaerium nucleofilum, which trap prey on axopodia radiating from the cell body. Microvideography showed that unicellular and colonial choanoflagellates entered the predator's capture zone at similar frequencies, but a greater proportion of colonies contacted axopodia. However, more colonies than single cells were lost during transport by axopodia to the cell body. Thus, feeding efficiency (proportion of prey entering the capture zone that were engulfed in phagosomes) was the same for unicellular and multicellular prey, suggesting that colony formation is not an effective defense against such passive predators.more » « less
-
Abstract Phenotypic features define feeding selectivity in planktonic predators and therefore determine energy flow through food webs. In current‐feeding cnidarian hydromedusae, swimming and predation are coupled such that swimming also brings prey into contact with feeding structures. Fluid mechanical disturbances may initiate escape responses by flow‐sensing prey. Previous studies have not considered how fluid signals define the trophic niche of current‐feeding gelatinous predators. We used the hydromedusaClytia gregariato determine (1) how passive (sinking) and active (swimming) feeding behavior affects pre‐encounter responses of prey to the medusae‐induced fluid motion, and (2) how prey responses affect the medusae's ingestion efficiencies. Videography of the predation process showed that passive prey such as invertebrate larvae were ingested during both feeding behaviors, whereas flow‐sensing prey such as copepods escaped the predator's active feeding behavior, but were unable to detect the predator's passive sinking behavior and were ingested (KWX2= 19.8246, df = 4,p < 0.001). Flow visualizations using particle image velocimetry (PIV) showed fluid deformation values during passive feeding below threshold values that trigger escape responses of copepods. To address whether fluid signals mediate prey capture, we compared fluid signals produced by three hydromedusae with different diets.Aequorea victoriaandMitrocoma cellulariaproduced higher deformation thanC. gregaria(two‐way ANOVA,F2,52= 5.532,p= 0.007), which explains their previously documented negative selection for flow‐sensing prey like copepods. Through the analysis of hydromedusan feeding behaviors and pre‐encounter prey escapes, we provide evidence that fluid signatures shape the trophic niches of gelatinous predators.more » « less
-
Abstract Lobate ctenophores are often numerically dominant members of oceanic epipelagic and midwater ecosystems. Despite this, little is known about their trophic ecology. Multiple, co‐occurring species are often found in these ecosystems and appear to feed similarly via feeding currents that entrain prey. We quantified the hydrodynamics, morphology, and behavior of four co‐occurring, cosmopolitan lobate species (Eurhamphaea vexilligera,Ocyropsis crystallina,Bolinopsis vitrea, andLeucothea multicornis) to evaluate whether their feeding mechanics lead to differential feeding rates and prey selection. We compared the feeding characteristics of these four oceanic species to the coastal lobate ctenophore,Mnemiopsis leidyi, which is known as a voracious zooplanktivore. We found that despite their morphological diversity, the five lobate species used the same mechanism to generate their feeding current—the hydrodynamics of their feeding currents were similarly laminar and with very low fluid deformation rates. Despite having similar feeding current traits, the species had different in situ swimming behaviors and feeding postures. We show that these different behaviors and postures lead to different prey encounter rates and that several of the oceanic species have the potential to feed at rates similar to or greater thanM. leidyi. As such, the individual and combined trophic impact of oceanic lobate ctenophores is likely to be much greater than previously predicted.more » « less
-
In this article, a porous hollow biotemplated nanoscale helix that can serve as a low Reynolds number robotic swimmer is reported. The nanorobot utilizes repolymerized bacterial flagella from Salmonella typhimurium as a nanotemplate for biomineralization. We demonstrate the ability to generate templated nanotubes with distinct helical geometries by using specific alkaline pH values to fix the polymorphic form of flagellar templates. Using uniform rotating magnetic fields to mimic the motion of the flagellar motor, we explore the swimming characteristics of these silica templated flagella and demonstrate the ability to wirelessly control their trajectories. The results suggest that the biotemplated nanoswimmer can be a cost-effective alternative to the current top-down methods used to produce helical nanorobots.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1017/flo.2023.16
