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

Stephen R. Fairclough, Zehua Chen, Eric Kramer, Qiandong Zeng, Sarah Young, Hugh M. Robertson, Emina Begovic, Daniel J. Richter, Carsten Russ, M. Jody Westbrook, Gerard Manning, B. Franz Lang, Brian Haas, Chad Nusbaum, Nicole King

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Pages (from-to)1-15
Number of pages15
JournalGenome biology
Volume14
Issue number2
DOIs
StatePublished - Feb 18 2013

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

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