Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta

Abstract

It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.

A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals

“…Although the original stock of S. rosetta (ATCC50818) was established from a rosette colony (Dayel et al 2011), laboratory cultures consistently produced single cells, with small numbers of rosette colonies forming only sporadically (Figure 1A, Figure 1—figure supplement 1). Serendipitously, we discovered that the bacterial community influences rosette colony development.…”

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

“…These SIT domains are not present in any of the sequenced non-siliceous choanoflagellate species [15,17,38,39], implying a correlation between their presence and lorica biomineralization.…”

Exploring the evolutionary history of centrosomes

“…Choanoflagellates can form long actin-based protrusions resembling filopodia required for attachment to the substrate but only exhibit flagellar motility [52,90]. The ultrastructure of choanoflagellates is also highly reminiscent of choanocytes, the feeding cells of sponges, which also assemble a collar of microvilli around the flagellum.…”

“…However, both Filasterea and animals exhibit actin-based motility, which suggests that their common ancestor was possibly undergoing amoeboid phases. In this scenario, choanoflagellates would have lost this trait secondarily, retaining filopodia only for attachment to the substrate [52,90]. The hypothesis that choanoflagellates are derived from ancestors with a more complex life cycle is not new [95,96].…”