Spatial Cell Disparity in the Colonial Choanoflagellate Salpingoeca rosetta

Abstract

Choanoflagellates are the closest unicellular relatives of animals (Metazoa). These tiny protists display complex life histories that include sessile as well as different pelagic stages. Some choanoflagellates have the ability to form colonies as well. Up until recently, these colonies have been described to consist of mostly identical cells showing no spatial cell differentiation, which supported the traditional view that spatial cell differentiation, leading to the co-existence of specific cell types in animals, evolved after the split of the last common ancestor of the Choanoflagellata and Metazoa. The recent discovery of single cells in colonies of the choanoflagellate Salpingoeca rosetta that exhibit unique cell morphologies challenges this traditional view. We have now reanalyzed TEM serial sections, aiming to determine the degree of similarity of S. rosetta cells within a rosette colony. We investigated cell morphologies and nuclear, mitochondrial, and food vacuole volumes of 40 individual cells from four different S. rosetta rosette colonies and compared our findings to sponge choanocytes. Our analysis shows that cells in a choanoflagellate colony differ from each other in respect to cell morphology and content ratios of nuclei, mitochondria, and food vacuoles. Furthermore, cell disparity within S. rosetta colonies is slightly higher compared to cell disparity within sponge choanocytes. Moreover, we discovered the presence of plasma membrane contacts between colonial cells in addition to already described intercellular bridges and filo-/pseudopodial contacts. Our findings indicate that the last common ancestor of Choanoflagellata and Metazoa might have possessed plasma membrane contacts and spatial cell disparity during colonial life history stages.

Keywords: cell differentiation; choanoflagellate; collar cells; evolution; multicellularity; sponge (Porifera).