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The Cellular and Molecular Basis of Multicellular Development in the Choanoflagellate Salpingoeca rosetta

Abstract

For more than a century and half choanoflagellates, the closest living relatives of animals, have fascinated evolutionary biologists. By characterizing the similarities and differences between choanoflagellates and animals, biologists have gained insight into their last common ancestor, the Urchoanimal. Understanding how choanoflagellates form multicelled colonies has important implications for understanding the cellular and evolutionary foundations of animal multicellularity. I determined that the colony forming choanoflagellate Salpingoeca rosetta forms colonies by cell division and not by cell aggregation. The observation that cytoplasmic bridges connect cells in S. rosetta colonies and other colonial choanoflagellates, as well as cells in sponges, suggests that this mechanism of colony formation may be ancestral within the choanoflagellate lineage and may have been present in the Urchoanimal as well. To understand the molecular mechanisms underlying S. rosetta colony formation and cellular differentiation, I analyzed the genome and transcriptome of S. rosetta. The comparison of choanoflagellate genomes with animal genomes has revealed that many of the genes involved in the basic mechanisms of cell adhesion, signaling, and differentiation that were previously thought to be unique to animals are present in choanoflagellates, indicating that these genes were present in the Urchoanimal. These insights also refine our understanding of genes that emerged on the stem lineage leading to the last common ancestor of all animals, the Urmetazoan. By characterizing patterns of gene expression in different cell types, in particular colonial cells, I determined that different cell types have unique patterns of gene expression suggesting there is transcriptional basis for the observed differentiation. By characterizing the set of genes that are expressed at higher levels in particular cell types, I discovered that septins, known regulators of cytokinesis, are over-expressed in colonial cells. I also found that subsets of the cadherin gene family, known for its role in intercellular adhesion and signaling, are over-expressed in colonial cells and attached cells. Taken together these data suggest that S. rosetta cells have a number of development trajectories, including multicellular colonies, whose biology involves homologs of animal genes operating in conserved and novel functions.

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