Rosette Colonies of Choanoflagellates (<i>Salpingoeca rosetta</i>) Show Increased Food Vacuole Formation Compared with Single Swimming Cells

L'Etoile, Nathan J.; King-Smith, Christina

doi:10.1111/jeu.12780

Cited by 6 publications

(4 citation statements)

References 16 publications

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“…Several selective factors have been proposed that might have favored the evolution of multicellularity in the ancestors of choanoflagellates and animals (reviewed by Koehl 2020). One suggestion is that multicellularity may have enhanced the rates at which cells in colonies captured bacterial prey (Kirkegaard and Goldstein 2016; L'Etoile and King-Smith 2020;Roper et al 2013;Stanley 1973). It has also been argued that an important selective factor leading to the evolution of multicellularity in the protozoan ancestors of animals was the relative difficulty that protozoan predators may have had in capturing larger multicellular colonies than smaller unicellular prey (Boraas et al 1998;Richter and King 2013;Stanley 1973).…”

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confidence: 99%

Does Formation of Multicellular Colonies by Choanoflagellates Affect Their Susceptibility to Capture by Passive Protozoan Predators?

Kumler

Jorge

Kim

et al. 2020

J Eukaryotic Microbiology

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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.

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confidence: 99%

Does Formation of Multicellular Colonies by Choanoflagellates Affect Their Susceptibility to Capture by Passive Protozoan Predators?

Kumler

Jorge

Kim

et al. 2020

J Eukaryotic Microbiology

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“…Because unicellular cyst-like cells seemed to have a survival advantage over multicellular flagellates in the hypersaline phase of the evaporation-refilling cycle, we wondered whether multicellularity, by contrast, was advantageous in the other phase of the cycle, marked by low salinity. It has been speculated that multicellularity in choanoflagellates might enhance feeding via cooperative hydrodynamic interactions between flagella, increasing the flux of bacterial prey towards the collar ( 75–77 ); however, this concept remains uncertain in the model choanoflagellate Salpingoeca rosetta , with different studies having come to contrasting conclusions ( 75 , 78 , 79 ). To test for a feeding advantage in multicellular sheets of C. flexa , we quantified the capture of fluorescent bacteria in sheets and dissociated single flagellates ( Figure 5B-C ).…”

Section: Resultsmentioning

confidence: 99%

Clonal-aggregative multicellularity entrained by salinity in one of the closest relative of animals

Ros-Rocher,

Reyes-Rivera,

Horo

et al. 2024

Preprint

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Multicellularity evolved multiple times independently during eukaryotic diversification. Two distinct mechanisms underpin multicellularity: clonal development (serial cell division of a single precursor cell) and aggregation (in which independent cells assemble into a multicellular entity). Clonal and aggregative development are traditionally considered to be mutually exclusive and to result from independent acquisitions of multicellularity. Here, we show that the choanoflagellate Choanoeca flexa, a close relative of animals that forms contractile monolayers of cells (or "sheet colonies"), develops by an unconventional intermediate mechanism that we name "clonal-aggregative multicellularity". We find that C. flexa sheets can form through purely clonal processes, purely aggregative processes, or a combination of both, depending on experimental conditions. To assess the ecological relevance of these findings, we characterize the natural context of multicellular development in the native environment of C. flexa on the island of Curaçao. We show that the C. flexa life cycle is environmentally regulated by extreme salinity fluctuations in splash pools undergoing cycles of evaporation and refilling. Upon desiccation, C. flexa colonies dissociate into drought-resistant quiescent cells, which resume activity and reform multicellular sheets after rehydration. We hypothesize that clonal-aggregative development reflects selection for fast transitions into and out of multicellularity in the ephemeral context of coastal splash pools. Our findings underscore the potential of the exploration of biodiversity to reveal new fundamental biological phenomena and expand the known option space for both multicellular development and for the origin of animal multicellularity.

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“…In contrast, Kirkegaard and Goldstein (2016) found no enhancement of flux for cells in chains or in rosette colonies (balls of cells with their flagella pointing outward) compared with unicellular choanoflagellates. Experiments showed no effect of multicellularity on feeding rates for choanoflagellates that form hemispherical colonies attached to the substratum by a stalk (Fenchel, 2019), whereas other studies revealed that freely swimming rosette colonies captured more bacteria per cell per time than did unicellular swimmers or unicellular thecate choanoflagellates attached to surfaces (Kreft, 2010; L'Etoile & King‐Smith, 2020). Measurements of choanoflagellate swimming showed that rosette colonies traveled more slowly than did unicellular choanoflagellates (Kirkegaard et al, 2016; Koehl, 2020), but water velocities measured relative to the collars of unicellular swimmers and of cells in rosette colonies showed that some of the cells in colonies encountered much greater water flux than did the single cells (Koehl, 2020).…”

Section: Discussionmentioning

confidence: 98%

Formation of multicellular colonies by choanoflagellates increases susceptibility to capture by amoeboid predators

Chin

O'Toole

et al. 2023

J Eukaryotic Microbiology

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Many heterotrophic microbial eukaryotes are size-selective feeders. Some microorganisms increase their size by forming multicellular colonies. We used choanoflagellates, Salpingoeca helianthica, which can be unicellular or form multicellular colonies, to study the effects of multicellularity on vulnerability to predation by the raptorial protozoan predator, Amoeba proteus, which captures prey with pseudopodia. Videomicrography used to measure the behavior of interacting S. helianthica and A. proteus revealed that large choanoflagellate colonies were more susceptible to capture than were small colonies or single cells. Swimming colonies produced larger flow fields than did swimming unicellular choanoflagellates, and the distance of S. helianthica from A. proteus when pseudopod formation started was greater for colonies than for single cells. Prey size did not affect the number of pseudopodia formed and the time between their formation, pulsatile kinematics and speed of extension by pseudopodia, or percent of prey lost by the predator. S. helianthica did not change swimming speed or execute escape maneuvers in response to being pursued by pseudopodia, so size-selective feeding by A. proteus was due to predator behavior rather than prey escape. Our results do not support the theory that the selective advantage of becoming multicellular by choanoflagellate-like ancestors of animals was reduced susceptibility to protozoan predation.

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Rosette Colonies of Choanoflagellates (Salpingoeca rosetta) Show Increased Food Vacuole Formation Compared with Single Swimming Cells

Cited by 6 publications

References 16 publications

Does Formation of Multicellular Colonies by Choanoflagellates Affect Their Susceptibility to Capture by Passive Protozoan Predators?

Does Formation of Multicellular Colonies by Choanoflagellates Affect Their Susceptibility to Capture by Passive Protozoan Predators?

Clonal-aggregative multicellularity entrained by salinity in one of the closest relative of animals

Formation of multicellular colonies by choanoflagellates increases susceptibility to capture by amoeboid predators

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