Open Access Research

Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta

Stephen R Fairclough1, Zehua Chen2, Eric Kramer3, Qiandong Zeng2, Sarah Young2, Hugh M Robertson4, Emina Begovic1, Daniel J Richter1, Carsten Russ2, M Jody Westbrook1, Gerard Manning3, B Franz Lang5, Brian Haas2, Chad Nusbaum2* and Nicole King1*

Author Affiliations

1 Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA 94720, USA

2 Broad Institute of MIT and Harvard, Cambridge, MA 02141, USA

3 Department of Computational Biology, Genentech, 1 DNA Way, South San Francisco, CA 94080, USA

4 Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

5 Departement de Biochimie, Universite de Montreal, Montreal, Quebec, Canada

For all author emails, please log on.

Genome Biology 2013, 14:R15  doi:10.1186/gb-2013-14-2-r15

Published: 18 February 2013

Abstract

Background

Metazoan multicellularity is rooted in mechanisms of cell adhesion, signaling, and differentiation that first evolved in the progenitors of metazoans. To reconstruct the genome composition of metazoan ancestors, we sequenced the genome and transcriptome of the choanoflagellate Salpingoeca rosetta, a close relative of metazoans that forms rosette-shaped colonies of cells.

Results

A comparison of the 55 Mb S. rosetta genome with genomes from diverse opisthokonts suggests that the origin of metazoans was preceded by a period of dynamic gene gain and loss. The S. rosetta genome encodes homologs of cell adhesion, neuropeptide, and glycosphingolipid metabolism genes previously found only in metazoans and expands the repertoire of genes inferred to have been present in the progenitors of metazoans and choanoflagellates. Transcriptome analysis revealed that all four S. rosetta septins are upregulated in colonies relative to single cells, suggesting that these conserved cytokinesis proteins may regulate incomplete cytokinesis during colony development. Furthermore, genes shared exclusively by metazoans and choanoflagellates were disproportionately upregulated in colonies and the single cells from which they develop.

Conclusions

The S. rosetta genome sequence refines the catalog of metazoan-specific genes while also extending the evolutionary history of certain gene families that are central to metazoan biology. Transcriptome data suggest that conserved cytokinesis genes, including septins, may contribute to S. rosetta colony formation and indicate that the initiation of colony development may preferentially draw upon genes shared with metazoans, while later stages of colony maturation are likely regulated by genes unique to S. rosetta.