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Saccharomyces cerevisiae: Oscillatory Orchestration of Growth

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Advancing Frontiers in Mycology & Mycotechnology

Abstract

It is important to understand the structure and function of Baker’s yeast as it serves as an excellent model, not only for many other fungi but also for almost all eukaryotic cell systems, including those of humans and hence biomedicine. In 1996, Saccharomyces cerevisiae became the first genetically defined eukaryotic organism to be sequenced: 6604 genes (> 400 orthologous with, and replaceable by human ones). Although its evolution has diverged for approximately 1.5 billion years from that of human cells, yeast research provides basic clues and insights into the molecular deficiencies and disorders of many human conditions: mitochondrial dysfunction, cellular division, apoptosis, diabetes, obesity, the accompaniments of old age, cancers, and “dynamic diseases” (neuropsychiatric conditions, e.g., many sleep disorders, depression). Dynamic maintenance of redox status and balanced energy supply and demand is crucial for optimum function and survival of yeast and of all cells. Recent advances in optoelectronics enable fast and continuous dynamic interrogation of processes in vivo. In this chapter, I outline the exquisite time order of molecular, metabolic, and biosynthetic events and processes that are organized with a precision that is commensurate with both spatial and temporal organization and that finds a coherence and resonance universally in life processes.

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References

  • Achs MJ, Kohn MC, Garfinkel (1979) Computer simulation of metabolism in pyruvate-perfused rat heart. IV. Model behavior. Am J Phys 237:R174–R180

    CAS  Google Scholar 

  • Adams CA, Kuriyama H, Lloyd D, Murray (2003) The Gts1 protein stabilizes the autonomous oscillator in yeast. Yeast 20:463–470

    Article  CAS  PubMed  Google Scholar 

  • Amariei C, Machné R, Stoic V, Soga T, Tomita M, Lloyd D, Murray DB (2013) Time resolved DNA occupancy dynamics during the respiratory oscillation uncover a global reset point in the yeast growth program. Microb Cell 1(9):279–288

    Article  CAS  Google Scholar 

  • Amariei C, Machné R, Sasidharan K, Gottstein W, Tomita M, Lloyd D, Murray DB (2014a) The dynamics of cellular energetics during continuous yeast culture. Conf Proc IEEE Eng Med Biol Soc 2013:2708–2711

    Google Scholar 

  • Amariei C, Tomita M, Murray DB (2014b) Quantifying periodicity in omics data. Front Cell Dev Biol 2:40. https://doi.org/10.3389/fcell.2014.00040

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersen AZ, Poulsen AK, Brasen JC, Olsen LF (2007) On-line measurements of oscillating mitochondrial membrane potential in glucose-fermenting Saccharomyces cerevisiae. Yeast 24:731–739

    Article  CAS  PubMed  Google Scholar 

  • Aon MA, Cortassa S (1997) Dynamic biological organization: fundamentals as applied to cellular systems. Springer, New York

    Book  Google Scholar 

  • Aon MA, Cortassa S, Lemar KM, Hayes A, Lloyd D (2007) Single and cell population respiratory oscillations in yeast: a 2-photon study. FEBS Lett 58:6–14

    Google Scholar 

  • Aon MA, Roussel MR, Cortassa S, O’Rourke B, Murray DB, Beckmann M, Lloyd D (2008a) The scale-free dynamics of eukaryotic cells. PLoS One 3(11):e3624

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aon MA, Cortassa S, O’Rourke B (2008b) Mitochondrial oscillations in physiology and pathophysiology. Adv Exp Med Biol 641:98–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aon MA, Cortassa S, Lloyd D (2011) Chaos in biochemistry and physiology. In: Meyers RA (ed) Encyclopedia of biochemistry and molecular cell biology and molecular medicine: systems biology, 2nd edn. Wiley-VCH Verlag, Weinheim, pp 239–276

    Google Scholar 

  • Aon MA, Lloyd D, Saks V (2014) From physiology, genomes, systems, self-organization to systems biology: the historical roots of a twenty-first century approach to complexity. In: Aon MA, Saks V, Schlattner U (eds) Systems biology of metabolic and signaling networks: energy, mass and information transfer. Springer, Berlin/Heidelberg, pp 3–17

    Chapter  Google Scholar 

  • Barnett JA (1998–2010). A history of research on yeasts: parts 1–14. Yeast 14:1439–1451 (1998) to 27: 875–904 (2010)

    Google Scholar 

  • Bashford CL, Poole RK, Lloyd D, Chance B (1980) Oscillations of redox state in synchronized dividing cultures of Acanthamoeba castellanii and Schizosaccharomyces pombe. Biophys J 29:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohátka S (1985) Quadrupole mass spectrometric measurement of dissolved and free gases. In: Degn H, Cox RP, Toflund H (eds) Gas enzymology. D. Reidel, Dordrecht, pp 1–16

    Google Scholar 

  • Bohátka S, Langer G, Szilágyi J, Berecz I (1983) Gas concentration determination in fermenters with quadrupole mass spectrometer. Int J Mass Spec Ion Phys 47:277–274

    Article  Google Scholar 

  • Boiteux A, Chance B (1970) Eighth Int Con Biochem, Luzern Abs

    Google Scholar 

  • Brodsky VY (1975) Protein synthesis rhythm. J Theor Biol 55:167–200

    Article  Google Scholar 

  • Brodsky VY (1992) Rhythms of protein synthesis and other cirahoralian oscilations: the possible involvement of fractals. In: Lloyd D, Rossi EL (eds) Ultradian rhythms in life processes. An inquiry into fundamental principles of chronobiology and psychology. Springer, London, pp 23–40

    Google Scholar 

  • Brodsky VY (2014) Circahoralian (ultradian) rhythms. Biochemistry (Mosc) 79(6):483–495

    Article  CAS  Google Scholar 

  • Cartledge TG, Lloyd D, Erecińska M, Chance B (1972) The development of the respiratory chain of Saccharomyces carlbergensis during respiratory adaptation. Biochem J 130:739–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvell J (2011) Creating new opportunities in process control through radio frequency impedence spectroscopy. BMC Proc 5(Suppl 8):P57

    PubMed  PubMed Central  Google Scholar 

  • Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134

    CAS  Google Scholar 

  • Chance B, Williamson G, Lee IY, Mela L, DeVault D, Ghosh AK, Pye EK (1973) Synchronization phenomena in oscillations in yeast cells and isolated mitochondria. In: Chance B, Pye EK, Ghosh AK, Hess B (eds) Biological and biochemical oscillators. A Colloquium of the Johnson Foundation. Academic, New York/London, pp 285–302

    Chapter  Google Scholar 

  • Chin SL, Marcus IM, Klevecz RR, Li CM (2012) Dynamics of oscillatory phenotypes in Saccharomyces cerevisiae reveal a network of genome-wide transcriptional oscillators. FEBS J 279:1119–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cortassa S, Aon MA, Marbán E, Winslow RL, O’Rourke (2003) An integrated model of cardiac mitochondrial metabolism. Biophys J 84:2734–2755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cortassa S, Aon MA, Iglesias AA, Aon JC, Lloyd D (2012) An introduction to metabolic and cellular engineering, 2nd edn. World Scientific, Singapore, pp xiv+ 428

    Google Scholar 

  • Dalal CK, Cai L, Lin Y, Rahbar K, Elowitz MB (2014) Pulsatile dynamics in the yeast proteome. Curr Biol 24(18):2189–2194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey HM, Davey CL, Woodward AM, Edmonds AN, Lee AW, Kell DB (1996) Oscillatory, stochastic and chaotic growth rate fluctuations in permittistatically controlled yeast cultures. Biosystems 39:43–61

    Article  CAS  PubMed  Google Scholar 

  • Degn H (1972) Oscillating chemical reactions in homogeneous phase. J Chem Educ 49:302–307

    Article  CAS  Google Scholar 

  • Dharmalingham, Jayaraman (1973) Mitochondriogenesis in synchronous cultures of yeast. I. Oscillatory pattern of respiration. Arch Biochem Biophys 157:197–202

    Article  Google Scholar 

  • Dunlap JC, Loros J (2017) Yes, circadian rhythms actually affect everything. Cell Res 26:759–760

    Article  CAS  Google Scholar 

  • Duysens LNM, Amesz J (1957) Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near ultraviolet and visible region. Biochem Biophys Acta 24:19–26

    Article  CAS  PubMed  Google Scholar 

  • Edmunds LN Jr (1980) Blue light photoreception in the inhibition and synchronization of growth and transport the yeast Saccharomyces. In: Senger H (ed) The blue light syndrome. Springer, Berlin, pp 584–596

    Chapter  Google Scholar 

  • Edwards SW, Lloyd D (1977) Mitochondrial adenosine triphosphate of the fission yeast Schizosaccharomyces pombe 972h. Biochem J 162:39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards SW, Lloyd D (1978) Oscillations of respiration and adenine nucleotides in synchronous cultures of Acanthamoeba castellanii: mitochondrial respiratory control in vivo. J Gen Microbiol 108:197–204

    Article  CAS  Google Scholar 

  • Edwards SW, Lloyd D (1980) Oscillations of protein and RNA content during synchronous growth of Acanthamoeba castellanii. FEBS Lett 109:21–26

    Article  CAS  PubMed  Google Scholar 

  • Edwards SW, Lloyd D (1982) The mitochondrial adenosine triphosphatase of Acanthamoeba castellanii: oscillatory accumulation of enzyme activity, enzyme protein and F1-inhibitor during the cell cycle. Biochem J 202:453–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards SW, Evans JB, Lloyd D (1981) Oscillatory accumulation of catalase during the cell cycle of Acanthamoeba castellanii. J Gen Microbiol 125:459–462

    CAS  Google Scholar 

  • Edwards SW, Evans JB, Williams JL, Lloyd D (1982) The mitochondrial adenosine triphosphatase of Acanthamoeba castellanii: oscillatory accumulation of enzyme activity, enzyme protein and F1-inhibitor during the cell cycle. Biochem J 202:453–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eelderink-Chen Z, Mazzotta G, Sturre M, Bosman J, Roenneberg T, Merrow M (2010) A circadian clock in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 107:2043–2047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eelderink-Chen Z, Olmedo M, Bosman J, Merrow M (2015) Chapter 4 – Using circadian entrainment to find cryptic clocks. Methods Enzymol 551:73–93

    Article  CAS  PubMed  Google Scholar 

  • Engelmann W, Bollig I, Hartmann R (1976) The effects of lithium ions on circadian rhythms. Arznemitteforschung 26(6):1085–1086

    CAS  Google Scholar 

  • Espeso EA (2016) The CRaZy calcium cycle. Adv Exp Med Biol 892:169–186

    Article  CAS  PubMed  Google Scholar 

  • Estabrook RW, Maitra PK (1962) A fluorimetric method for the quantitative analysis of adenine and pyridine nucleotides. Anal Biochem 3:369–382

    Article  CAS  PubMed  Google Scholar 

  • Fricker MD, Tlalka M, Bebber D, Tagaki S, Watkinson SC, Darrah PR (2007) Fourier-based spatial mapping of oscillatory phenomena in fungi. Fungal Genet Biol 44(11):1077–1084

    Article  CAS  PubMed  Google Scholar 

  • Ghosh AK, Chance B (1964) Oscillation of glycolytic intermediates in yeast cells. Biochem Biophys Res Commun 16:174–181

    Article  CAS  PubMed  Google Scholar 

  • Goodwin BC (1963) Analytical physiology of cells and developing organisms: a dynamic theory of cellular control processes. Academic, London/New York, pp x+249

    Google Scholar 

  • Heimburg T (2017) Linear nonequilibrium thermodynamics of reversible periodic processes and chemical oscillations. Phys Chem Chem Phys 19:17331–19341

    Article  CAS  PubMed  Google Scholar 

  • Hess B, Bioteux A (1971) Oscillatory phenomena in biochemistry. Annu Rev Biochem 53:237–258

    Article  Google Scholar 

  • Higgins J, Frenkel R, Hulme E, Lucas A, Rangazas (1973) The control theoretic approach to the analysis of glycolytic oscillators. In: Chance B, Pye EK, Ghosh AK, Hess B (eds) Biological and biochemical oscillators. A Colloquium of the Johnson Foundation. Academic, New York/London, pp 127–175

    Chapter  Google Scholar 

  • Hughes ME, DiTacchio, Hayes KR et al (2009) Harmonics of circadian gene transcripts. PLoS Genet 5(4):e1000442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hughes ME, Arbruzzi KC, Allada R et al (2017) Guidelines for genome-scale analysis of biological rhythms. J Biol Rhythm 32:380–393

    Article  CAS  Google Scholar 

  • Jules M, François J, Parrou JL (2005) Autonomous oscillations in Saccharomyces cerevisiae during cultures on trehalose. FEBS J 272:1490–1500

    Article  CAS  PubMed  Google Scholar 

  • Jules M, Beltran G, François J, Parrou JL (2007) New insights into trehalose metabolism by NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Appl Environ Microbiol 74(3):605–613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kader J, Lloyd D (1979) Respiratory oscillations and heat evolution in synchronous cultures of Candida utilis. J Gen Microbiol 114:455–461

    Article  CAS  PubMed  Google Scholar 

  • Keulers M, Kuriyama H (1998) Extracellular signaling in an yeast culture. In: Holcombe WLM, Paton R, Holcombe M (eds) Information processing in cells and tissues. Plenum, New York, pp 85–94

    Chapter  Google Scholar 

  • Keulers M, Satroutdinov AD, Kuriyama H (1996a) Oscillations in ethanol grown Saccharomyces cerevisiae. FEBS Microbiol Lett 142:253–258

    Article  CAS  Google Scholar 

  • Keulers M, Satroutdinov AD, Suzuki T, Kuriyama H (1996b) Synchronization affector of autonomous short-period-sustained oscillation of Saccharomyces cerevisiae. Yeast 12:673–682

    Article  CAS  PubMed  Google Scholar 

  • Kippert F (1997) Lithium affects the ultradian clock of Schizosaccharomyces pombe by inhibition of inositol monophosphatase. Biochem Soc Trans 25(4):S602

    Article  CAS  PubMed  Google Scholar 

  • Kippert F (2001) Cellular signaling and the complexity of biological timing: insights from the ultradian clock of Schizosaccharomyces pombe. Phil Trans Roy Soc Lond B Biol Sci 356:1725–1733

    Article  CAS  Google Scholar 

  • Kippert F, Lloyd D (1995) A temperature-compensated clock ticks in Schizosaccharomyces pombe. Microbiology 141:883–890

    Article  CAS  PubMed  Google Scholar 

  • Kippert F, Engelmann W, Ninnemann H (1990) Blue light synchronizes and inhibits the growth of Schizosaccharomyces pombe. Prog Clin Biol Res 341B:271–280

    CAS  PubMed  Google Scholar 

  • Klevecz RR (1976) Quantized generation times in mammalian cells as an expression of the cellular clock. Proc Natl Acad Sci U S A 73:4012–4016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klevecz RR (1992) A precise circadian clock from chaotic cell cycle oscillations. In: Lloyd D, Rossi EL (eds) Ultradian rhythms in life processes. An inquiry into fundamental principles of chronobiology and psychology. Springer, London, pp 41–69

    Google Scholar 

  • Klevecz RR, Li CM (2007) Evolution of the clock from yeast to man by period-doubling folds. Cold Spring Harb Symp Quant Biol 72:421–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klevecz RR, Murray DB (2001) Genome wide oscillations: wavelet analysis of time series analysis in yeast expression arrays uncovers the dynamic architecture of phenotype. Mol Biol Rep 28:73–82

    Article  CAS  PubMed  Google Scholar 

  • Klevecz RR, Bolen J, Forest G, Murray DB (2004) A genome-wide oscillation in transcription gates DNA replication and the cell cycle. Proc Natl Acad Sci U S A 101:1200–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klevecz RR, Li CM, Marcus I, Frankel PH (2008) Collective behavior in gene regulation: the cell is an oscillator, the cell cycle a developmental process. FEBS J 275:2372–2384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar N (1996) Deterministic chaos: complex chance out of simple necessity. University Press (India), Jawaharlal Nehru Centre for Advanced Research, Hyderabad, pp xi+96

    Google Scholar 

  • Kurz FT, Kembro JM, Flesia AG, Armoundas AA, Cortassa S, Aon MA, Lloyd D (2017) Network dynamics: quantitative analysis of complex behavior in metabolism, organelles, and cells, from experiments to models and back. Wiley Interdiscip Rev Syst Biol Med 9(1). https://doi.org/10.1002/wsbm.1352

    Google Scholar 

  • Kwak WJ, Kwong GS, Jin I, Kuriyama H, Sohn HY (2003) Involvement of oxidative stress in the regulation of H2S production during ultradian metabolic oscillation of Saccharomyces cerevisiae. FEBS Microbiol Lett 219:99–104

    Article  CAS  Google Scholar 

  • Lemar KM (2003) Cell death mechanisms in the human opportunistic pathogen, Candida albicans. J Eukaryot Microbiol 50(Suppl):685–686

    Article  CAS  PubMed  Google Scholar 

  • Lemar KM, Passa O, Aon MA, Cortassa S, Muller CT, Plummer S, O’Rourke B, Lloyd D (2005) Allyl alcohol and garlic (Allium sativum) produce oxidative stress in Candida albicans. Microbiology 151:3257–3265

    Article  CAS  PubMed  Google Scholar 

  • Lemar KM, Aon MA, Cortassa S, O’Rourke B, Muller CT, Lloyd D (2007) Diallyl disulphide depletes glutathione in Candida albicans : oxidative-stress mediated cell death studied by two-photon microscopy. Yeast 24:695–706

    Article  CAS  PubMed  Google Scholar 

  • Li LZ (2011) Special section in memory of Professor Britton Chance: celebrating the life and legasy of Britton Chance. J Innov Optical Health Sci 4(2):v–vii

    Article  Google Scholar 

  • Li CM, Klevecz RR (2006) A rapid genome-scale response to the transcriptional oscillator to perturbation reveals a period-doubling path to phenotypic change. Proc Natl Acad Sci U S A 103:16254–16259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Grant GR, Hogenesch JB, Hughes ME (2015) Chapter sixteen-considerations for RNA-seq analysis of circadian rhythms. Methods Enzymol 551:349–367

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D (2003) Effects of uncoupling of mitochondrial energy conservation on thevultradian clock-driven oscillations in Saccharomyces cerevisiae continuous culture. Mitochondrion 3:139–146

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D (2006) The ultradian clock: not to be confused with the cell cycle. Nat Rev Mol Cell Biol 7. https://doi.org/10.1038/hrm1980-cl

  • Lloyd D (2009) Oscillations, synchrony and deterministic chaos. In: Lüttge U, Beyschlag W, Büdel B, Francis D (eds) Progress in botany, vol 70. Springer, Berlin, pp 69–92

    Chapter  Google Scholar 

  • Lloyd D (2016) Biological timekeeping: the business of a blind watchmaker. Sci Prog 99(2):113–132

    Article  CAS  Google Scholar 

  • Lloyd D, Edwards SW (1977) Mitochondrial adenosine triphosphate of the fission yeast Schizosaccharomyces pombe 972h. Biochem J 162:581–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd D, Kippert F (1993) Intracellular coordination by the ultradian clock. Cell Biol Int 17:1047–1052

    Article  CAS  PubMed  Google Scholar 

  • Lloyd AL, Lloyd D (1992) Hypothesis: the central oscillator of the circadian clock is a controlled chaotic attractor. Biosystems 29:77–85

    Article  Google Scholar 

  • Lloyd AL, Lloyd D (1995) Chaos: its detection and significance in biology. Biol Rhythm Res 26:233–252

    Article  Google Scholar 

  • Lloyd D, Murray DB (2000) Redox cycling of intracellular thiols: state variables for ultradian, cell division and circadian cycles. In: Van den Driessche T, Guisset JL, DeVries GP (eds) Redox behaviour of Circadian systems. Kluwer, Amsterdam, pp 85–94

    Chapter  Google Scholar 

  • Lloyd D, Murray DB (2005) Ultradian metronome: timekeeper for orchestration of cellular coherence. Trends Biochem Sci 30(7): 373–377

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Murray DB (2007) Redox rhythmicity: clocks at the core of temporal coherence. Bioessays 29:465–473

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Stupfel M (1991) The occurrence and functions of ultradian rhythms. Biol Rev 66:275–299

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, John L, Edwards C, Chagla AH (1975) Establishment of large scale synchronous cultures of microorganisms by continuous flow size selection. J Gen Microbiol 88:153–158

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, John L, Hamill M, Phillips C, Kader J, Edwards SW (1977) Continuous-flow cell cycle fractionation of eukaryotic microorganisms. J Gen Microbiol 99:223–227

    Article  Google Scholar 

  • Lloyd D, Boveris A, Reiter R, Filipkowski M, Chance B (1979) Chemiluminescence of Acanthamoeba castellanii. Biochem J 184:149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd D, Edwards SW, Williams JL (1981) Oscillatory accumulation of total cellular protein in Candida utilis. FEMS Microbiol Lett 12:295–298

    Article  CAS  Google Scholar 

  • Lloyd D, Poole RK, Edwards SW (1982a) The cell division cycle: temporal organization and control of cellular growth and reproduction. Academic, London, pp xii+513

    Google Scholar 

  • Lloyd D, Edwards SW, Fry JC (1982b) Temperature-compensated oscillations in respiration and cellular protein in synchronous cultures of Acanthamoeba castellanii. Proc Natl Acad Sci U S A 79:3785–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd D, Kristensen B, Degn H (1983a) Glycolysis and respiration in yeasts: the Pasteur effect studied by mass spectrometry. Biochem J 212:749–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd D, Edwards SW, Williams JL, Evans JB (1983b) Mitochondrial cytochromes of Acanthamoeba castellanii: oscillatory accumulation haemoproteins, immunological determinants and activity during the cell cycle. FEMS Microbiol Lett 16:307–312

    Article  CAS  Google Scholar 

  • Lloyd D, Bohátka S, Szilágyi J (1985) Quadrupole mass spectrometry in the monitoring and control of fermentations. Biosensors 1:179–212

    Article  CAS  Google Scholar 

  • Lloyd D, Lloyd AL, Olsen LF (1992) The cell division cycle: a physiologically plausible dynamic model can exhibit chaotic solutions. Biosystems 27:17–24

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Thomas K, Price D, O’Neill W, Oliver K, Williams TN (1996) A MIMS miniprobe for the direct simultaneous measurement of multiple gas species. J Microbiol Methods 25:145–151

    Article  CAS  Google Scholar 

  • Lloyd D, Salgado LE, Turner MP, Murray DB (2002a) Respiratory oscillations in yeast: clock-driven mitochondrial cycles of energization. FEBS Lett 519:41–44

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Salgado LEJ, Turner MP, Suller MTE, Murray DB (2002b) Cycles of mitochondrial energization driven by the ultradian clock in a culture of Saccharomyces cerevisiae. Microbiology 148:3715–3724

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Murray DB, Klevecz RR, Wolf J, Kuriyama H (2008) The ultradian clock (~ 40 min) in yeast. In: Lloyd D, Rossi EL (eds) Ultradian rhythms from molecules to mind: a new vision of life. London, Springer, pp 11–42

    Google Scholar 

  • Lloyd D, Cortassa S, O’Rourke B, Aon MA (2012) What yeast and cardiomyocytes share: ultradian oscillatory redox mechanisms of cellular coherence and survival. Integr Biol (Camb) 4:65–74

    Article  CAS  Google Scholar 

  • Lobo Z, Maitra PK (1983) Genetics of yeast glucokinase. Genetics 105:501–515

    PubMed  PubMed Central  Google Scholar 

  • Luzikov VN (1984). Mitochondrial biogenesis and breakdown (trans. Galkin AV, Roodyn DB). Consultants Bureau, New York/London

    Google Scholar 

  • Luzikov VN (2009) Principles of control over formation of structures responsible for respiratory functions of mitochondria. Biochem Mosc 74:1443–1456

    Article  CAS  Google Scholar 

  • Machné R, Murray DB (2012) The yin and yang of yeast transcription : elements of a global feedback system between metabolism and chromatin. PLoS One 7(6):e37906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Machné R, Murray DB, Stadler PF (2017) Similarity-based segmentation of multi-dimensional signals. Sci Rep 7(1):12355

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maitra PK (1966) Pulsating glucose flux in yeast. Biochem Biophys Res Commun 25:462–467

    Article  CAS  PubMed  Google Scholar 

  • Maitra PK (1971) Glucose and fructose metabolism in a phosphoglucoisomeraseless mutant of Saccharomyces cerevisiae. J Bacteriol 107:759–769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maitra PK, Estabrook RW (1964) A fluorimetric method for the enzymic determination of glycolytic intermediates. Anal Biochem 7:472–484

    Article  CAS  PubMed  Google Scholar 

  • Male T, Feder J, Giaever GN, Giaever I (1999) Oscillations in yeast observed electrically. Biol Rhythm Res 30(4):361–370

    Article  Google Scholar 

  • Merrow M, Raven M (2010) Finding time: a daily clock in yeast. Cell Cycle 9:1671–1672

    Article  CAS  PubMed  Google Scholar 

  • Mochan E, Pye K (1973) Respiratory oscillations in adapting yeast cultures. Nat New Biol 242:177–179

    Article  CAS  PubMed  Google Scholar 

  • Murray DB (2004) On the temporal organization of Saccharomyces cerevisiae. Curr Genom 5:665–671

    Article  CAS  Google Scholar 

  • Murray DB (2006) The respiratory oscillation in yeast: phase definitions and periodicity. Nature Rev Mol Cell Biol 7. https://doi.org/10.1038/hrm1980-cl

  • Murray AW, Kirschner MW (1989) Dominoes and clocks: the union of two views of the cell cycle. Science 246:914–621

    Article  Google Scholar 

  • Murray DB, Lloyd D (2005) Ultradian metronome: timekeeper for orchestration of cellular coherence. Trends Biochem Sci 30:373–377

    Article  PubMed  CAS  Google Scholar 

  • Murray DB, Lloyd D (2006) A tunable attractor underlies yeast respiratory dynamics. Biosystems 90:287–294

    Article  PubMed  CAS  Google Scholar 

  • Murray DB, Engelen FA, Keulers M, Kuriyama H, Lloyd D (1999a) NO+ but not NO inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae. FEBS Lett 431:297–299

    Article  Google Scholar 

  • Murray DB, Engelen FA, Keulers M, Kuriyama H, Lloyd D (1999b) NO+ but not NO inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae. Biochem Soc Trans 26(4):S339

    Article  Google Scholar 

  • Murray DB, Keuler M, Englen F, Lloyd D, Kuriyama H (1999c) Involvement of glutathione in the regulation of respiratory oscillation during a continuous culture of Saccharomyces cerevisiae. Microbiology 145:2739–2745

    Article  CAS  PubMed  Google Scholar 

  • Murray DB, Roller S, Kuriyama H, Lloyd D (2001) Clock control of respiratory oscillations found during yeast continuous culture. J Bacteriol 183:7253–7259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray DB, Klevecz RR, Lloyd D (2003) Generation and maintenance of synchrony in Saccharomyces cerevisiae continuous culture. Exp Cell Res 287:10–15

    Article  CAS  PubMed  Google Scholar 

  • Murray DB, Beckmann M, Kitano H (2007) Regulation of yeast oscillatory dynamics. Proc Natl Acad Sci U S A 104:2241–2246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray DB, Haynes K, Tomita T (2011) Redox regulation in respiring Saccharomyces cerevisiae. Biochim Biophys Acta 1819:845–958

    Google Scholar 

  • Murray DB, Amariei C, Sasidharan K, Machne R, Aon MA, Lloyd D (2014) Temporal partitioning of the yeast cellular network. In: Aon MA, Saks V, Schlattner U (eds) Systems biology of metabolic and signaling networks: energy, mass and information transfer, Springer series in biophysics, 16. Springer, Berlin/Heidelberg, pp 323–349

    Chapter  Google Scholar 

  • Ninnemann H (1995) Some aspects of blue light research. Photochem Photobiol 61:22–31

    Article  CAS  PubMed  Google Scholar 

  • Ninnemann H, Butler WL, Epel BL (1970) Inhibition of respiration in yeast by light. Biochem Biophys Acta 205:499–506

    CAS  PubMed  Google Scholar 

  • Nosoh Y, Takamiya A (1962) Synchronisation of budding cycle in yeast cells and effect of carbon monoxide and nitrogen deficiency on the synchrony. Plant Cell Physiol 3:59–66

    Google Scholar 

  • Ohnishi T, Cartledge TG, Lloyd D (1972) The development of mitochondrial iron-sulphur protens during the respiratory adaptation of Saccharomyces carlsbergensis. FEBS Lett 52:90–94

    Article  Google Scholar 

  • Olsen LF, Andersen AZ, Lunding A, Brasen JC, Poulsen AK (2009) Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases. Biophys J 96:3850–3861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palková Z, Váchová L (2016) Mitochondria in aging cell differentiation. Aging 8(7):1287–1288

    Article  PubMed  PubMed Central  Google Scholar 

  • Palková Z, Devaux F, Icicová M, Mináriková L, Le Crom S, Jacq C (2002) Ammonia pulses and metabolic oscillations guide yeast colony development. Mol Biol Cell 13:3901–3914

    Article  PubMed  PubMed Central  Google Scholar 

  • Papagiannakis A, Niebel B, Wit EC, Heinemann M (2017) Autonomous metabolic oscillations robustly gate the early and late cell cycle. Mol Cell 65:285–295

    Article  CAS  PubMed  Google Scholar 

  • Picard M, McManus MJ, Gray JD, Nasca C, Moffat C, Kopinski PK, Seifert EL, McEwen BS, Wallace DC (2015) Mitochondrial functions modulate neuroendocrine, metabolic, inflammatory and transcriptional responses to acute psychological stress. Proc Natl Acad Sci U S A 112(48):E6614–E6623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Picard M, Wallace DC, Burelle Y (2016) The rise of mitochondria in medicine. Mitochondrion 30:105–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plavskii VY, Mikulich AV, Tretyakova AI et al (2018) Porphyrins and flavins are endogenous acceptors of optical radiation determining photoinactivation of microbial cells. J Photochem Photobiol 183:172–183

    Article  CAS  Google Scholar 

  • Poole RK, Lloyd D (1973) Changes in enzyme activities in synchronously dividing cultures of Schizosaccharomyces pombe h. Biochem J 136:195–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poole RK, Lloyd D, Kemp RB (1973) Respiratory oscillations and heat evolution in synchronous cultures of fission yeast, Schizosaccharomyces pombe 972 h. J Gen Microbiol 77:209–290

    Article  Google Scholar 

  • Poole RK, Lloyd D, Chance B (1974) The development of the cell division cycle of a glucose-repressed fission yeast, Schizosaccharomyces pombe 972 h. Biochem J 138:201–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen AK, Andersen AZ, Brasen JC, Scharff-Poulsen AM, Olsen LF (2008) Probing glycolytic and membrane potential oscillations in Saccharomyces cerevisiae. Biochemistry 47:7477–7484

    Article  CAS  PubMed  Google Scholar 

  • Rapkine L (1931) Sur les processes chimiques au course de la division cellulaire. Ann Physiol Physicochem 7:382–418

    CAS  Google Scholar 

  • Rensing L, Meyer-Grahl U, Ruoff P (2001) Biological timing and the clock metaphor: oscillatory and hour-glass mechanisms. Chronobiol Int 18:329–369

    Article  CAS  PubMed  Google Scholar 

  • Roussel MR, Lloyd D (2007) Observation of a chaotic multi-oscillatory metabolic attractor by real-time monitoring of a yeast continuous culture. FEBS J 274:1011–1018

    Article  CAS  PubMed  Google Scholar 

  • Salgado EL, Murray DB, Lloyd D (2002) Some antidepressants (Li+, monoamine oxidase type- A inhibitors) perturb the ultradian clock in Saccharomyces cerevisiae. Biol Rhythm Res 33:351–361

    Article  CAS  Google Scholar 

  • Sasidharan K, Soga T, Tomita M, Murray DB (2012a) A yeast metabolite extraction protocol optimized for time-series analyses. PLoS One 7:e44283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasidharan K, Amariei C, Tomita M, Murray DB (2012b) Rapid DNA, RNA and protein extraction protocols optimized for slow continuously growing yeast cultures. Yeast 29:311–322

    Article  CAS  PubMed  Google Scholar 

  • Sasidharan K, Tomita M, Aon MA, Lloyd D, Murray DB (2012c) The time-structure of yeast metabolism in vivo. In: Goryanin I, Goryachev A (eds) Advances in systems biology. Springer, New York

    Google Scholar 

  • Satroutdinov AD, Kuriyama H, Kobayashi H (1992) Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. FEMS Microbiol Lett 98:261–268

    Article  CAS  Google Scholar 

  • Silverman SJ, Petti AA, Slavov N, Parsond L, Briehof R, Thiberge S, Zenklusen D, Gandhi SJ, Larson DR, Singer RH, Botstein DP (2010) Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate. Proc Natl Acad Sci U S A 107:6946–6951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slavov N, Botstein D (2011) Coupling among groth rate response, metabolic cycle and cell division cycle in yeast. Mol Biol Cell 22:1997–2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slavov N, Macinskas J, Caudy A, Botstein D (2011) Metabolic cycling without cell division in respiring yeast. Proc Natl Acad Sci U S A 108:19090–19095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sohn HY, Murray DB, Kuriyama H (2000) Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulfide mediates population synchrony. Yeast 16:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Thoke HS, Tobiesen A, Brewer J, Hansen PL, Stock RP, Olsen LF, Bagatolli LA (2015) Tight coupling of metabolic oscillations and intracellular water dynamics. PLoS One 10:e0117308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thoke HS, Thorsteinsson S, Stock RP, Bagatolli LA, Olsen LF (2017) The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae. Sci Rep 7:16250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thoke HS, Olsen LF, Duelund L, Stock RP, Heimburg T, Bagatolli LA (2018) Is a constant low-entropy process at the root of glycolytic oscillations? J Biol Phys 44:419–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu BP, McKnight SL (2006) Metabolic cycles as an underlying basis of biological oscillations. Nature Rev Mol Cell 7:696–701

    Article  CAS  Google Scholar 

  • Tu BP, Kudlicki A, Rowika M, McKnight SL (2005) Logic of the cell metabolic cycle: temporal compartmentation of cellular processes. Science 310:1152–1158

    Article  CAS  PubMed  Google Scholar 

  • Ułaszewski S, Mamouneas T, Shen W-K, Rosenthal OJ, Woodward JR, Cirillo VP, Edmunds LN Jr (1979) Light effects in yeast: evidence for participation of cytochromes in photoinhibition of Saccharomyces cerevisiae cultured at low temperatures. J Bacteriol 138:523–529

    PubMed  PubMed Central  Google Scholar 

  • Wallace DC (2012) Mitochondria and cancer. Nat Rev Cancer 12:685–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace DC (2015) Mitochondrial DNA in human variation and disease. Cell 163:33–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiemken A, von Meyenburg HK, Matile P (1970) Properties of the vacuole in baker’s yeast synchronized with a new method. Acta Fac Med Uni Brunensis 37:47–52

    Google Scholar 

  • Wille JJ Jr (1974) Light entrained circadian oscillations of growth rate in the yeast Candida utilis. In: Scheving LE, Halberg F, Pauly JE (eds) Chronobiology. Igaku Shoin, Tokyo, pp 72–77

    Google Scholar 

  • Woodward JR, Cirillo VP, Edmunds LN Jr (1978) Light effects in yeast: inhibition by visible light of growth and transport in Saccharomyces cerevisiae grown at low temperatures. J Bacteriol 133:692–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z, Tsurugi K (2007a) Role of Gts1 in regulation of energy-metabolism oscillation in continuous cultures of the yeast Saccharomyces cerevisiae. Yeast 24:161–170

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Tsurugi K (2007b) De-stabilisation of energy-metabolism oscillation in the absence of trehalose synthesis in the chemostat culture of yeast. Arch Biochem Biophys 464(2):350–358

    Article  CAS  PubMed  Google Scholar 

  • Xu HN, Tchou J, Feng M, Zhao H, Li LZ (2016) Optical redox imaging indices discriminate human breast cancer from normal tissues. J Biomed Opt 21(11):114003

    Article  PubMed  PubMed Central  Google Scholar 

  • Yates FE (1982) Outline of a physical theory of physiological systems. Can J Physiol Pharmacol 60:217–248

    Article  CAS  PubMed  Google Scholar 

  • Yates FE (1992) Fractal applications in biology: scaling time in biochemical networks. In: Brand L, Johnson ML (eds) Numerical methods, methods enzymol, vol 210. Academic, New York, pp 636–676

    Google Scholar 

  • Yates FE (1993) Self-organizing systems. In: Boyd CAR, Noble D (eds) The logic of life: the challenge of integrative physiology. Oxford University Press, Oxford, pp 189–218

    Google Scholar 

  • Yates FE, Yates LB (2008) Ultradian rhythms as the signatures of life. In: Lloyd D, Rossi EL (eds) Ultradian rhythms from molecules to mind, a new vision of life. Springer, Dordrecht, pp 249–260

    Chapter  Google Scholar 

  • Zand K, Pham T, Davila A Jr, Wallace DC, Burke PJ (2013) Nanofluidic platform for single mitochondria analysis using fluorescence microscopy. Anal Chem 85(12):6018–6025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

DL would like to thank all the students and coworkers for permission to summarize their contribution to work on temporal organization of the growth of yeasts.

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Lloyd, D. (2019). Saccharomyces cerevisiae: Oscillatory Orchestration of Growth. In: Satyanarayana, T., Deshmukh, S., Deshpande, M. (eds) Advancing Frontiers in Mycology & Mycotechnology. Springer, Singapore. https://doi.org/10.1007/978-981-13-9349-5_7

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