Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery

PLoS Genet. 2020 Mar 16;16(3):e1008584. doi: 10.1371/journal.pgen.1008584. eCollection 2020 Mar.


Progression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures the just-in-time gene expression. Many core cell cycle regulators are widely conserved in eukaryotes, among them cyclins and CDKs; however, periodic transcriptional programs are divergent between distantly related species. In addition, many otherwise conserved cell cycle regulators have been lost and independently evolved in yeast, a widely used model organism for cell cycle research. For a better understanding of the evolution of the cell cycle regulation in opisthokonts, we investigated the transcriptional program during the cell cycle of the filasterean Capsaspora owczarzaki, a unicellular species closely related to animals. We developed a protocol for cell cycle synchronization in Capsaspora cultures and assessed gene expression over time across the entire cell cycle. We identified a set of 801 periodic genes that grouped into five clusters of expression over time. Comparison with datasets from other eukaryotes revealed that the periodic transcriptional program of Capsaspora is most similar to that of animal cells. We found that orthologues of cyclin A, B and E are expressed at the same cell cycle stages as in human cells and in the same temporal order. However, in contrast to human cells where these cyclins interact with multiple CDKs, Capsaspora cyclins likely interact with a single ancestral CDK1-3. Thus, the Capsaspora cyclin-CDK system could represent an intermediate state in the evolution of animal-like cyclin-CDK regulation. Overall, our results demonstrate that Capsaspora could be a useful unicellular model system for animal cell cycle regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle / genetics*
  • Cells, Cultured
  • Cyclin-Dependent Kinases / genetics*
  • Cyclins / genetics
  • Eukaryota / genetics*
  • Gene Expression / genetics
  • Saccharomyces cerevisiae / genetics
  • Transcription, Genetic / genetics
  • Transcriptome / genetics*


  • Cyclins
  • Cyclin-Dependent Kinases

Grant support

This work was funded by a European Research Council Consolidator Grant (ERC-2012-Co-616960) to IRT; and a grant from the Spanish Ministry for Economy and Competitiveness (MINECO; BFU2017-90114-P, with European Regional Development Fund support) to IRT. AP was supported by a “la Caixa” Foundation (ID 100010434) fellowship, whose code is LCF/BQ/ES16/11570008. OD was supported by a Swiss National Science Foundation Early PostDoc Mobility fellowship (P2LAP3_171815) and a Marie Sklodowska-Curie individual fellowship (MSCA-IF 746044). EOP was supported by a pre-doctoral FPI grant from MINECO. AO was supported by a Marie Sklodowska-Curie individual fellowship (MSCA-IF 747086). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.