Choanoflagellates with inversion

Salpingoeca rosetta

Figure 1A from Dayel et al. 2011. Spherical colony of Salpingoeca rosetta. Scale bar = 5 μm.

The closest (known) living relatives of animals are a group of unicellular or colonial filter-feeders known as choanoflagellates. Much of what we know about the evolution of multicellularity in animals comes from comparisons with choanoflagellates. For example, many of the gene families involved in multicellular development in animals, and previously thought to be unique to animals, have turned out to be present in choanoflagellates as well, suggesting that these gene families were present in animal ancestors before they evolved multicellularity. Some multicellular choanoflagellates have even been shown to have differentiated cell types (Laundon et al. 2019):

Choanoflagellate cell differentiation

Figure 3M from Laundon et al. 2019. 3D ssTEM reconstructions of five complete rosettes of the choanoflagellate Salpingoeca rosetta(RC1–5) coloured by cell number (above), and 2D projections of bridge connections in 3D ssTEM reconstructions of RCs (below). Asterisks mark the presence of highly derived cell morphologies in RC3 and RC4.

Now a choanoflagellate has been shown to perform another animal trick: collective cell contractions. Thibaut Brunet and colleagues found a new colonial choanoflagellate on the Caribbean island of Curaçao and found that it undergoes inversion in response to changing light conditions. The new choano, Choanoeca flexa, forms cup-shaped colonies that switch between a “flagella-in” and a “flagella-out” conformation:

Choanoeca flexa

Figure 1E & F from Brunet et al. 2019. Choanoeca flexa colonies in the “flagella-in” (E) and “flagella-out” (F) conformations.

The “flagella-in” conformation is triggered by light and is more efficient at feeding, while the “flagella-out” conformation is triggered by darkness and is better at swimming. The authors suggest that this scheme may result in effective phototaxis, with slower-swimming “flagella-in” colonies accumulating in bright areas, and in fact they found that Choanoeca flexa colonies do tend to move toward a light source.

The inversion process in Choanoeca flexa colonies is a bit reminiscent of the process of “partial inversion” in Gonium, but the similarities are pretty shallow. Both Gonium and Choaneca flexa invert from a “flagella-in” to a “flagella-out” conformation, and in both cases there is reason to think that this improves motility. However, in Gonium inversion is a one-time event that occurs during embryogenesis, and it’s a one-way trip. Choanoeca flexa colonies switch back and forth in response to changing light conditions, and they presumably do this many time throughout their lives. Furthermore, the mechanics of the process are fundamentally different. Gonium inverts through a combination of changes in cell shape and expansion of the concave surface:

Gonium inversion

Figure S5a from Yamashita & Nozaki 2019. Embryogenesis in Gonium pectorale based on time-lapse microscopy. Each cell of a vegetative colony performed four successive cell divisions to form a cup-shaped 16-celled embryo with basal bodies positioned in the center of the concave surface of the cell layer. The cell layer of the embryo expanded gradually after successive cell divisions and instantly upon hatching of the daughter colony, with the basal bodies moving from the center to the periphery of the cell layer.

Choaneca flexa, on the other hand, inverts through changes in the opening angle of the collar microvilli that connect the cells:

inversion in Choaneca flexa.

Figure 5U from Brunet et al. 2019. Mechanism of inversion in Choaneca flexa.

So although Gonium and Choaneca flexa both undergo inversion, the similarities are superficial. Their most recent common ancestor was almost certainly unicellular, so inversion in these two lineages is an example of convergent evolution. The similarity between the contractions that drive inversion in Choaneca flexa and contractions that occur during animal development, though, go much deeper. Brunet and colleagues found that the contraction of the collar microvilli involves actomyosin, a protein complex involved in cell movements, including muscle contraction, in animals. It’s nearly certain, then, that the unicellular ancestor of animals and choanoflagellates also had actomyosin.

Even more surprisingly, the mechanism of light detection in Choaneca flexa also has a parallel in animals. Brunet and colleagues found that the inversion response to light depends on rhodopsin, a light-sensitive pigment used in the rod cells of animal retinas. Just like animals, choanoflagellates lack the ability to synthesize a precursor of rhodopsin, retinal, and have to get it (or another precursor, β-carotene) from their food. Brunet and colleagues demonstrated the dependence of Choaneca flexa inversion on diet with an elegant experiment: they deprived the choanoflagellates of their normal bacterial prey, which produce rhodopsin precursors, and fed them instead on a species of bacteria that does not. Colonies cultured this way did not invert in response to changing light conditions, and they only regained this ability when retinal was added to their medium.

So we can add contraction using actomyosin and light detection using rhodopsin to the list of “animal” traits that probably were present in an ancestor we shared with choanoflagellates. The authors conclude with a reminder that much remains unknown about this newly discovered species:

Much remains to be discovered concerning the ecological function, mechanical underpinnings, and molecular mechanisms of phototransduction and apical constriction in C[hoaneca] flexa. A deeper understanding will require the development of molecular genetic tools, which have only recently been established in [the model choanoflagellate] S[alpingoeca] rosetta and D[iaphanoeca] grandis. [references omitted]

and of the value of understanding the biology of multiple related species:

Nonetheless, C[hoaneca] flexa demonstrates how the exploration of choanoflagellate diversity can reveal biological phenomena and provides an experimentally tractable model for studying multicellular sensory-contractile coupling.

I couldn’t agree more. We have gained immense benefits from studying a few model species selected, at least in part, for their experimental tractability. What this focus has gained us in depth, though, has been partly offset by a cost in breadth. By expanding our view to the lesser-known relatives of model organisms, which technological advances have made much easier in recent years, we stand to learn new biology and comparative context.

Choaneca flexa colonies undergoing inversion (Supplemental Movie S1 from Brunet et al. 2019):

More about inverting choanoflagellates on This Week in Evolution


Stable links:

Brunet, T., B. T. Larson, T. A. Linden, M. J. A. Vermeij, K. McDonald, and N. King. 2019. Light-regulated collective contractility in a multicellular choanoflagellate. Science 366:326–334. doi: 10.1126/science.aay2346

Dayel, M. J., R. A. Alegado, S. R. Fairclough, T. C. Levin, S. A. Nichols, K. McDonald, and N. King. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Developmental Biology 357:73–82. doi: 10.1016/j.ydbio.2011.06.003

Laundon, D., B. T. Larson, K. McDonald, N. King, and P. Burkhardt. 2019. The architecture of cell differentiation in choanoflagellates and sponge choanocytes. PLOS Biology 17:e3000226. doi: 10.1371/journal.pbio.3000226

Yamashita, S., and H. Nozaki. 2019. Embryogenesis of flattened colonies implies the innovation required for the evolution of spheroidal colonies in volvocine green algae. BMC Evolutionary Biology 19:120. doi: 10.1186/s12862-019-1452-x


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