Evolutionary history of “tissue-bending”

This (developmental biology) story is an awesome example of gene-environment interactions. 😊 To start with, animal embryos shape their tissues during development through a variety of mechanisms — one of which involves coordinated constriction of one side of a sheet of embryonic cells, leading to tissue bending. This constriction mechanism during tissue morphogenesis occurs in most animal groups, suggesting evolutionarily that it was inherited from a common ancestor. Authors [see attached article and editorial] describe a remarkable discovery of a new species of colony-forming unicellular eukaryote — which uses collective cell contraction to change its morphology and behavior in response to absence of light. Because the new species belongs to the closest living relatives of animals (i.e. the choanoflagellates), these results cast new light on the evolutionary origin of collective cell contractility.

In a pond on the island of Curaçao, authors found an intriguing creature composed of ~100 cells — with whip-like appendages (flagellae) that together formed a small sheet; the sheet was bent inward, with the flagellae pointing toward the interior of a cup-shaped colony. However, occasionally the sheet would invert its curvature rapidly, and — within 30 seconds — all the flagellae would be facing outward along the radius of the inverted colony [shown in Fig. 1 of article and in diagram on p. 301 of editorial].

This dramatic and quick change in tissue morphology is similar to developmental morphogenesis in complex multicellular animals (including human embryos), in which epithelial sheets fold and invaginate to form multilayered structures. Authors concluded that this organism is a new species of choanoflagellate and named it Choanoeca flexa. Authors managed to keep their C. flexa alive in the laboratory — by growing it in the presence of the bacteria on which it fed in the pond where it was discovered. What happened next is an example of scientific curiosity, clever thinking, and elucidation of mechanism…!!

Authors found that “the inversion behavior” is triggered by switching off the light. Analysis of the C. flexa genome revealed a gene encoding the protein rhodopsin phosphodiesterase, which both “senses” light, and “passes the information on” to other cellular processes by modifying cyclic nucleotides commonly used in intracellular signaling. This gene was a good candidate to explain the observed light-dependent behavior, but how does one prove this premise? Authors knew that photodetection via rhodopsin requires a cofactor — the chromophore retinal, but C. flexa does not have the genes necessary to produce retinal. Therefore, it must be taking up retinal from food, the bacteria. Authors fed their choanoflagellates with bacteria that can, or cannot, produce retinal, and they found that only C. flexa colonies feeding on retinal-producing bacterial strains can “invert” in response to the environmental signal, “darkness”. Moreover, addition of synthetic retinal alone — was also able to trigger the inversion.

Lastly, what does “inversion” of this multicellular colony accomplish for C. flexa? Authors showed that — when the cell colony has its flagellae facing inward — it can consume the bacteria better by capturing them from the surrounding medium. When the creature “inverts”, however, its flagellae are oriented in a way that’s more useful for mobility of the colony (probably to escape a large predator casting a shadow over the colony). Therefore, the sheet inversion appears to mediate a trade-off between feeding and swimming to avoid a predator. This really amazing story might be helpful in reconstructing hypothesized animal ancestors that existed before the evolution of specialized sensory and contractile cells. 😊


Science 18 Oct 2019; 366: 326-334 & editorial pp 300-301

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