Nutritional homeostasis in batch and steady-state culture of yeast.

We studied the physiological response to limitation by diverse nutrients in batch and steady-state (chemostat) cultures of S. cerevisiae. We found that the global pattern of transcription in steady-state cultures in limiting phosphate or sulfate is essentially identical to that of batch cultures growing in the same medium just before the limiting nutrient is completely exhausted. The massive stress response and complete arrest of the cell cycle that occurs when nutrients are fully exhausted in batch cultures is not observed in the chemostat, indicating that the cells in the chemostat are "poor, not starving." Similar comparisons using leucine or uracil auxotrophs limited on leucine or uracil again showed patterns of gene expression in steady-state closely resembling those of corresponding batch cultures just before they exhaust the nutrient. Although there is also a strong stress response in the auxotrophic batch cultures, cell cycle arrest, if it occurs at all, is much less uniform. Many of the differences among the patterns of gene expression between the four nutrient limitations are interpretable in light of known involvement of the genes in stress responses or in the regulation or execution of particular metabolic pathways appropriate to the limiting nutrient. We conclude that cells adjust their growth rate to nutrient availability and maintain homeostasis in the same way in batch and steady state conditions; cells in steady-state cultures are in a physiological condition normally encountered in batch cultures.

[1]  Andrew Hayes,et al.  Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  B Marshall,et al.  Gene Ontology Consortium: The Gene Ontology (GO) database and informatics resource , 2004, Nucleic Acids Res..

[3]  Erin K O'Shea,et al.  Partially Phosphorylated Pho4 Activates Transcription of a Subset of Phosphate-Responsive Genes , 2003, PLoS biology.

[4]  J. Townsend,et al.  BMC Genomics BioMed Central Methodology article , 2003 .

[5]  G. Kohlhaw Leucine Biosynthesis in Fungi: Entering Metabolism through the Back Door , 2003, Microbiology and Molecular Biology Reviews.

[6]  J. Pronk,et al.  The Genome-wide Transcriptional Responses of Saccharomyces cerevisiae Grown on Glucose in Aerobic Chemostat Cultures Limited for Carbon, Nitrogen, Phosphorus, or Sulfur* , 2003, The Journal of Biological Chemistry.

[7]  J. Warner,et al.  Autoregulation in the Biosynthesis of Ribosomes , 2003, Molecular and Cellular Biology.

[8]  David Botstein,et al.  The Stanford Microarray Database: data access and quality assessment tools , 2003, Nucleic Acids Res..

[9]  Kevin Dobbin,et al.  Comparison of microarray designs for class comparison and class discovery , 2002, Bioinform..

[10]  N. D. Clarke,et al.  Rationalization of gene regulation by a eukaryotic transcription factor: calculation of regulatory region occupancy from predicted binding affinities. , 2002, Journal of molecular biology.

[11]  J. Pronk,et al.  Reproducibility of Oligonucleotide Microarray Transcriptome Analyses , 2002, The Journal of Biological Chemistry.

[12]  T. Speed,et al.  Design issues for cDNA microarray experiments , 2002, Nature Reviews Genetics.

[13]  Margaret Werner-Washburne,et al.  The genomics of yeast responses to environmental stress and starvation , 2002, Functional & Integrative Genomics.

[14]  Andrew Hayes,et al.  Hybridization array technology coupled with chemostat culture: Tools to interrogate gene expression in Saccharomyces cerevisiae. , 2002, Methods.

[15]  E. O’Shea,et al.  Pho85 and signaling environmental conditions. , 2002, Trends in biochemical sciences.

[16]  P. Reichard Ribonucleotide reductases: the evolution of allosteric regulation. , 2002, Archives of biochemistry and biophysics.

[17]  Kara Dolinski,et al.  Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO) , 2002, Nucleic Acids Res..

[18]  J. Heijnen,et al.  Statistical reconciliation of the elemental and molecular biomass composition of Saccharomyces cerevisiae. , 2001, Biotechnology and bioengineering.

[19]  D. Botstein,et al.  Genomic expression programs in the response of yeast cells to environmental changes. , 2000, Molecular biology of the cell.

[20]  P. Brown,et al.  New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. , 2000, Molecular biology of the cell.

[21]  D. Botstein,et al.  Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Duboc,et al.  An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. , 2000, Enzyme and microbial technology.

[23]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[24]  M. Tyers,et al.  SCFMet30‐mediated control of the transcriptional activator Met4 is required for the G1–S transition , 2000 .

[25]  M. Tyers,et al.  SCF(Met30)-mediated control of the transcriptional activator Met4 is required for the G(1)-S transition. , 2000, The EMBO journal.

[26]  M. Ashburner,et al.  The Gene Ontology Consortium , 2000 .

[27]  Ronald W. Davis,et al.  Genome-Wide Transcriptional Analysis of Aerobic and Anaerobic Chemostat Cultures of Saccharomyces cerevisiae , 1999, Journal of bacteriology.

[28]  B. Persson,et al.  Phosphate permeases of Saccharomyces cerevisiae: structure, function and regulation. , 1999, Biochimica et biophysica acta.

[29]  J. Warner,et al.  The economics of ribosome biosynthesis in yeast. , 1999, Trends in biochemical sciences.

[30]  Dake Wang,et al.  Yeast Transcriptional Regulator Leu3p , 1999, The Journal of Biological Chemistry.

[31]  M. G. Koerkamp,et al.  Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. , 1999, Molecular biology of the cell.

[32]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Michael Ruogu Zhang,et al.  Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. , 1998, Molecular biology of the cell.

[34]  Karl-Dieter Entian,et al.  23 Yeast Mutant and Plasmid Collections , 1998 .

[35]  Y. Surdin-Kerjan,et al.  Metabolism of sulfur amino acids in Saccharomyces cerevisiae , 1997, Microbiology and molecular biology reviews : MMBR.

[36]  P. Brown,et al.  Exploring the metabolic and genetic control of gene expression on a genomic scale. , 1997, Science.

[37]  S. Carr,et al.  Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. , 1997, Science.

[38]  C. Scazzocchio,et al.  A single amino acid change in a pathway-specific transcription factor results in differing degrees of constitutivity, hyperinducibility and derepression of several structural genes. , 1995, Journal of molecular biology.

[39]  E. O’Shea,et al.  Phosphate-regulated inactivation of the kinase PHO80-PHO85 by the CDK inhibitor PHO81. , 1994, Science.

[40]  G. Géraud,et al.  Endocytosis and degradation of the yeast uracil permease under adverse conditions. , 1994, The Journal of biological chemistry.

[41]  M. Denis-Duphil Pyrimidine biosynthesis in Saccharomyces cerevisiae: the ura2 cluster gene, its multifunctional enzyme product, and other structural or regulatory genes involved in de novo UMP synthesis. , 1989, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[42]  Y. Surdin-Kerjan,et al.  SAM2 encodes the second methionine S-adenosyl transferase in Saccharomyces cerevisiae: physiology and regulation of both enzymes , 1988, Molecular and cellular biology.

[43]  R. Losson,et al.  Yeast promoters URA1 and URA3. Examples of positive control. , 1985, Journal of molecular biology.

[44]  J. Davies,et al.  Molecular Biology of the Cell , 1983, Bristol Medico-Chirurgical Journal.

[45]  C. Yanofsky,et al.  Translational coupling during expression of the tryptophan operon of Escherichia coli. , 1980, Genetics.

[46]  A. Nowotny Microdetermination of Phosphorus , 1979 .

[47]  Jacques Monod,et al.  LA TECHNIQUE DE CULTURE CONTINUE THÉORIE ET APPLICATIONS , 1978 .

[48]  L. Hartwell Saccharomyces cerevisiae cell cycle. , 1974, Bacteriological reviews.

[49]  A. Novick,et al.  Description of the chemostat. , 1950, Science.

[50]  J. Monod,et al.  Recherches sur la croissance des cultures bactériennes , 1942 .