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The Ultradian Clock (~40 min) in Yeast (Saccharomyces cerevisiae)

  • D. Lloyd
  • D. B. Murray
  • R. R. Klevecz
  • J. Wolf
  • H. Kuriyama

Abstract

A precisely controlled, continuously grown, aerobic yeast culture system shows an autonomous sustained respiratory oscillation (i.e. a high amplitude change in dissolved O2 levels: the residual O2 that remains after the organisms use what they require). This spontaneously organized synchronous state can be maintained for extended periods (months) and continuously monitored for intracellular redox state (by direct fluorimetric output for nicotinamide nucleotides: excitation 366 nm, emission 450 nm), and dissolved gases (O2 electrode and/or direct membrane inlet mass spectrometry for O2, CO2 and H2S, sampled on a 15s cycle). The whole culture population (~5 × 108 organisms/ml) is behaving metabolically as if it were a single cell, so that analysis for metabolic intermediates (keto and amino-acids, carboxylic acids), redox components (glutathione, cysteine, NAD(P)H and reactive O2 species) and products (acetaldehyde, acetic acid and ethanol), with sampling at frequent time intervals gives reliable information on phase relationships on the approximately 40min ultradian cycle. Lipid peroxidation levels indicate the changing levels of oxidative stress. Microarray analysis shows a genome-wide oscillation in transcription, with expression maxima at three nearly equally spaced intervals on the 40min time-base. The first temporal cluster (4,679 of 5,329 genes expressed) occurred maximally during the reductive phase, whereas the remaining 650 transcripts were detected maximally in the oxidative phase. Furthermore, when fixed samples of yeasts were analysed for DNA using flow cytometry, synchronous bursts in the initiation of DNA replication (occurring in about 8% of the total population) were shown to coincide with decreasing respiration rates. A precisely defined appearance of mitochondrial energy generation-dependent conformational changes, the machinery for protein synthesis and degradation and for mitochondrial ribosome assembly are also all locked on the ultradian clock cycle phase. This indicates the pervasive and all-embracing nature of temporal co-ordination of cellular growth and division. The major players in this yeast model system are identified as some of the most highly conserved components common to all eukaryotes. Thus a primeval, fundamental and insistent drum-beat reverberates in all eukaryotic systems, in microbes, animals and plants. The ultradian clock that co-evolved with increasing atmospheric O2 predates and underpins the circadian clock at the central core of endogenous intracellular timekeeping. It represents the prototype of all biological rhythmicity: circadian clocks evolved much more recently, almost as the icing on the cake.

Keywords

Yeast self-synchrony respiration redox state metabolic switch transcriptional regulation cell division cycle ultradian clock 

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Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • D. Lloyd
    • 1
  • D. B. Murray
    • 2
  • R. R. Klevecz
    • 3
  • J. Wolf
    • 4
  • H. Kuriyama
    • 5
  1. 1.Microbiology (BIOSI 1)Cardiff School of BiosciencesCardiffWales, UK
  2. 2.Institute for Advanced BiosciencesKeio UniversityYamagataJapan
  3. 3.Dynamics Group, Department of BiologyBeckman Research Institute of the City of Hope Medical CenterDuarteUSA
  4. 4.Humboldt-UniversityGermany
  5. 5.Biochemical Engineering Lab.National Institute of Advanced Industrial Science and Technology, AISTIbarakiJapan

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