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Peroxiredoxins are conserved markers of circadian rhythms

Nature volume 485, pages 459–464 (2012)Cite this article

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A Corrigendum to this article was published on 08 August 2012

Abstract

Cellular life emerged ∼3.7 billion years ago. With scant exception, terrestrial organisms have evolved under predictable daily cycles owing to the Earth’s rotation. The advantage conferred on organisms that anticipate such environmental cycles has driven the evolution of endogenous circadian rhythms that tune internal physiology to external conditions. The molecular phylogeny of mechanisms driving these rhythms has been difficult to dissect because identified clock genes and proteins are not conserved across the domains of life: Bacteria, Archaea and Eukaryota. Here we show that oxidation–reduction cycles of peroxiredoxin proteins constitute a universal marker for circadian rhythms in all domains of life, by characterizing their oscillations in a variety of model organisms. Furthermore, we explore the interconnectivity between these metabolic cycles and transcription–translation feedback loops of the clockwork in each system. Our results suggest an intimate co-evolution of cellular timekeeping with redox homeostatic mechanisms after the Great Oxidation Event ∼2.5 billion years ago.

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Figure 1: The peroxiredoxin active site is highly conserved in all domains of life.
Figure 2: Peroxiredoxin oxidation cycles are conserved in eukaryotic models of the circadian clock.
Figure 3: Peroxiredoxin oxidation cycles are conserved in prokaryotic models of the circadian clock.
Figure 4: Peroxiredoxin oxidation cycles in circadian clock mutants.
Figure 5: Relationships between peroxiredoxins and the cyanobacterial Kai-based oscillator.
Figure 6: Phylogenetic origins of circadian oscillatory systems.

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Acknowledgements

This work was primarily supported by the Wellcome Trust (083643/Z/07/Z and 093734/Z/10/Z), the European Research Council (ERC Starting Grant No. 281348, MetaCLOCK), and EMBO Young Investigators Programme, as well as the Medical Research Council Centre for Obesity and Related metabolic Disorders (MRC CORD), and the National Institute for Health Research (NIHR) Cambridge Biomedical Research Centre. C.P.K. and M.H.H. acknowledge European Commission grant EUCLOCK (no. 018741) and Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/C006941/1. SynthSys is funded by BBSRC and Engineering and Physical Sciences Research Council (EPSRC) award BB/D019621 to A.J.M. and others. N.S.B. was supported by ENIGMA, US Department of Energy, under contract no. DE-AC02-05CH11231, and by a grant from the National Institutes of Health (NIH; P50GM076547). C.H.J. was supported by the NIH (R01GM088595, R01GM067152 and R21HL102492). M.M. was supported by the Netherlands Organisation for Scientific Research (NWO; Dutch Science Foundation VICI award and Open Programma) and the University of Groningen (Rosalind Franklin Fellowship Program). We thank M. Jain, G. O’Neill and J. Chambers for discussion about the manuscript, and S. G. Rhee, F. Rouyer and R. Stanewsky for the gifts of antisera.

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  1. Rachel S. Edgar, Edward W. Green, Yuwei Zhao, Gerben van Ooijen and Maria Olmedo: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Neurosciences, University of Cambridge Metabolic Research Laboratories, NIHR Biomedical Research Centre, Institute of Metabolic Science, University of Cambridge, Addenbrooke’s Hospital, Cambridge CB2 0QQ, UK,

    Rachel S. Edgar, Utham K. Valekunja, Kevin A. Feeney, John S. O’Neill & Akhilesh B. Reddy

  2. Department of Genetics, University of Leicester, Leicester LE1 7RH, UK,

    Edward W. Green & Charalambos P. Kyriacou

  3. Department of Biological Sciences, Vanderbilt University, Nashville, 37235-1634, Tennessee, USA

    Yuwei Zhao, Ximing Qin, Yao Xu & Carl H. Johnson

  4. Synthetic and Systems Biology (SynthSys), Mayfield Road, Edinburgh EH9 3JD, UK ,

    Gerben van Ooijen & Andrew J. Millar

  5. Department of Molecular Chronobiology, Center for Life Sciences, University of Groningen, 9700 CC Groningen, The Netherlands,

    Maria Olmedo & Martha Merrow

  6. Institute for Systems Biology, 401 Terry Avenue North, Seattle, 98109, Washington, USA

    Min Pan & Nitin S. Baliga

  7. MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK ,

    Elizabeth S. Maywood & Michael H. Hastings

  8. School of Biological Sciences, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JR, UK ,

    Andrew J. Millar

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  1. Rachel S. Edgar
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Contributions

A.B.R. and J.S.O. conceived and designed the experiments, and wrote the manuscript. R.S.E., E.W.G., G.v.O., M.O., X.Q., Y.X., Y.Z., M.P., U.K.V., K.A.F. and E.S.M. performed experiments. M.H.H., N.S.B., C.H.J., M.M., A.J.M. and C.P.K. provided reagents. R.S.E., E.W.G., G.v.O., M.O. and Y.Z. contributed equally to this work.

Corresponding authors

Correspondence to John S. O’Neill or Akhilesh B. Reddy.

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Edgar, R., Green, E., Zhao, Y. et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459–464 (2012). https://doi.org/10.1038/nature11088

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