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Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

Author

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  • Coralie Fumeaux

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

  • Sunish Kumar Radhakrishnan

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1
    Present address: Indian Institute of Science Education and Research, CET campus, Thiruvananthapuram 695016, Kerala, India)

  • Silvia Ardissone

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

  • Laurence Théraulaz

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

  • Antonio Frandi

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

  • Daniel Martins

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

  • Jutta Nesper

    (Biozentrum of the University of Basel, Klingelbergstrasse 50/70)

  • Sören Abel

    (Biozentrum of the University of Basel, Klingelbergstrasse 50/70
    Present address: Division of Infectious Diseases, Department of Microbiology and Immunobiology, Brigham and Women’s Hospital, Harvard Medical School, 181 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Urs Jenal

    (Biozentrum of the University of Basel, Klingelbergstrasse 50/70)

  • Patrick H. Viollier

    (Faculty of Medicine/CMU, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Rue Michel Servet 1)

Abstract

Zinc-finger domain transcriptional regulators regulate a myriad of functions in eukaryotes. Interestingly, ancestral versions (MucR) from Alpha-proteobacteria control bacterial virulence/symbiosis. Whether virulence regulators can also control cell cycle transcription is unknown. Here we report that MucR proteins implement a hitherto elusive primordial S→G1 transcriptional switch. After charting G1-specific promoters in the cell cycle model Caulobacter crescentus by comparative ChIP-seq, we use one such promoter as genetic proxy to unearth two MucR paralogs, MucR1/2, as constituents of a quadripartite and homeostatic regulatory module directing the S→G1 transcriptional switch. Surprisingly, MucR orthologues that regulate virulence and symbiosis gene transcription in Brucella, Agrobacterium or Sinorhizobium support this S→G1 switch in Caulobacter. Pan-genomic ChIP-seq analyses in Sinorhizobium and Caulobacter show that this module indeed targets orthologous genes. We propose that MucR proteins and possibly other virulence regulators primarily control bacterial cell cycle (G1-phase) transcription, rendering expression of target (virulence) genes periodic and in tune with the cell cycle.

Suggested Citation

  • Coralie Fumeaux & Sunish Kumar Radhakrishnan & Silvia Ardissone & Laurence Théraulaz & Antonio Frandi & Daniel Martins & Jutta Nesper & Sören Abel & Urs Jenal & Patrick H. Viollier, 2014. "Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators," Nature Communications, Nature, vol. 5(1), pages 1-14, September.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms5081
    DOI: 10.1038/ncomms5081
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