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PLoS Biol. 2019 Apr 12;17(4):e3000226. doi: 10.1371/journal.pbio.3000226. eCollection 2019 Apr.

The architecture of cell differentiation in choanoflagellates and sponge choanocytes.

Author information

1
Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, United Kingdom.
2
Plymouth University, Drake Circus, Plymouth, United Kingdom.
3
Biophysics Graduate Group, University of California, Berkeley, Berkeley, California, United States of America.
4
Electron Microscope Laboratory, University of California, Berkeley, Berkeley, California, United States of America.
5
Department of Molecular and Cell Biology, University of California, Berkeley, United States of America.
6
Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, California, United States of America.
7
Sars International Centre for Molecular Marine Biology, University of Bergen, Bergen, Norway.

Abstract

Although collar cells are conserved across animals and their closest relatives, the choanoflagellates, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal development and can alternate between unicellular and multicellular states, making it a powerful model for investigating the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular 'rosette' colonies and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with higher levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks, and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type, pointing toward spatial cell differentiation. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some but not all neighbouring cells. Reconstruction of sponge choanocytes revealed ultrastructural commonalities but also differences in major organelle composition in comparison to choanoflagellates. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of animals.

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