Physiological and transcriptional responses of anaerobic chemostat cultures of Saccharomyces cerevisiae subjected to diurnal temperature cycles

Applied and Environmental Microbiology

Volumn 80, Issue 14, 2014, Pages 4433-4449

  Hebly, Marit ^a,b,c   de Ridder, Dick ^a,b,d   de Hulster, Erik A F ^a,b   Cortes, Pilar de la Torre ^a,b   Pronk, Jack T ^a,b,c   Daran Lapujade, Pascale ^a,b,c  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^c Netherlands Consortium for Systems Biology   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CARBON DIOXIDE; CELLS; CHEMOSTATS; CYTOLOGY; ENZYME ACTIVITY; GENES; GLUCOSE; PHYSIOLOGICAL MODELS; PHYSIOLOGY; TEMPERATURE DISTRIBUTION;

DIURNAL TEMPERATURE CYCLES; EXTRACELLULAR METABOLITES; INTRINSIC CHARACTERISTICS; PARTIAL SYNCHRONIZATION; SINUSOIDAL TEMPERATURE; TEMPERATURE-RESPONSIVE; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL RESPONSE;

YEAST;

ANOXIC CONDITIONS; CONCENTRATION (COMPOSITION); DIURNAL VARIATION; GENOME; GLUCOSE; METABOLITE; PHYSIOLOGICAL RESPONSE; TEMPERATURE EFFECT; YEAST;

CULTURE MEDIUM; GLUCOSE; TRANSCRIPTOME;

ADAPTATION; ANAEROBIC GROWTH; CHEMISTRY; CULTURE MEDIUM; ECOSYSTEM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; SACCHAROMYCES CEREVISIAE; TEMPERATURE;

ADAPTATION, PHYSIOLOGICAL; ANAEROBIOSIS; CULTURE MEDIA; ECOSYSTEM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GLUCOSE; PRINCIPAL COMPONENT ANALYSIS; SACCHAROMYCES CEREVISIAE; TEMPERATURE; TRANSCRIPTOME;

EID: 84903155479     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00785-14     Document Type: Article

References (88)

1. Madigan MT, Martinko JM. 2006. Brock biology of microorganisms. Prentice Hall, Upper Saddle River, NJ.
2. Feller G, Gerday C. 2003. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 1:200-208. http://dx.doi.org/10.1038 /nrmicro773.
3. Thieringer HA, Jones PG, Inouye M. 1998. Cold shock and adaptation. Bioessays 20:49-57.
4. Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D. 2004. Control of membrane lipid fluidity by molecular thermosensors. J. Bacteriol. 186: 6681-6688. http://dx.doi.org/10.1128/JB.186.20.6681-6688.2004.
5. Schumann W. 2009. Temperature sensors of eubacteria. Adv. Appl. Microbiol. 67:213-256. http://dx.doi.org/10.1016/S0065-2164(08)01007-1.
6. Gasch AP, Werner-Washburne M. 2002. The genomics of yeast responses to environmental stress and starvation. Funct. Integr. Genomics 2:181-192. http://dx.doi.org/10.1007/s10142-002-0058-2.
7. Dragosits M, Stadlmann J, Albiol J, Baumann K, Maurer M, Gasser B, Sauer M, Altmann F, Ferrer P, Mattanovich D. 2009. The effect of temperature on the proteome of recombinant Pichia pastoris. J. Proteome Res. 8:1380-1392. http://dx.doi.org/10.1021/pr8007623.
8. Gunnigle E, McCay P, Fuszard M, Botting CH, Abram F, O'Flaherty V. 2013. A functional approach to uncover the low-temperature adaptation strategies of the archaeon Methanosarcina barkeri. Appl. Environ. Microbiol. 79:4210-4219. http://dx.doi.org/10.1128/AEM.03787-12.
9. Marr AG, Ingraham JL. 1962. Effect of temperature on the composition of fatty acids in Escherichia coli. J. Bacteriol. 84:1260-1267.
10. Jones PG, Inouye M. 1994. The cold-shock response-a hot topic. Mol. Microbiol. 11:811-818. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00359.x.
11. Al-Fageeh MB, Smales CM. 2006. Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem. J. 397:247-259. http://dx.doi.org/10.1042/BJ20060166.
12. Lindquist S. 1986. The heat-shock response. Annu. Rev. Biochem. 55: 1151-1191. http://dx.doi.org/10.1146/annurev.bi.55.070186.005443.
13. Klinkert B, Narberhaus F. 2009. Microbial thermosensors. Cell. Mol. Life Sci. 66:2661-2676. http://dx.doi.org/10.1007/s00018-009-0041-3.
14. Postmus J, Canelas AB, Bouwman J, Bakker BM, van Gulik WM, de Mattos MJT, Brul S, Smits GJ. 2008. Quantitative analysis of the high temperature-induced glycolytic flux increase in Saccharomyces cerevisiae reveals dominant metabolic regulation. J. Biol. Chem. 283:23524-23532. http://dx.doi.org/10.1074/jbc.M802908200.
15. Salvado Z, Arroyo-Lopez FN, Guillamon JM, Salazar G, Querol A, Barrio E. 2011. Temperature adaptation markedly determines evolution within the genus Saccharomyces. Appl. Environ. Microbiol. 77:2292-2302. http://dx.doi.org/10.1128/AEM.01861-10.
16. Redon M, Guillamon JM, Mas A, Rozes N. 2011. Effect of growth temperature on yeast lipid composition and alcoholic fermentation at low temperature. Eur. Food Res. Technol. 232:517-527. http://dx.doi.org/10.1007/s00217-010-1415-3.
17. Lodolo EJ, Kock JL, Axcell BC, Brooks M. 2008. The yeast Saccharomyces cerevisiae-the main character in beer brewing. FEMS Yeast Res. 8:1018-1036. http://dx.doi.org/10.1111/j.1567-1364.2008.00433.x.
18. Pizarro FJ, Jewett MC, Nielsen J, Agosin E. 2008. Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 74:6358-6368. http://dx.doi.org/10.1128/AEM.00602-08.
19. Sasano Y, Haitani Y, Hashida K, Oshiro S, Shima J, Takagi H. 2013. Improvement of fermentation ability under baking-associated stress conditions by altering the POG1 gene expression in baker's yeast. Int. J. Food Microbiol. 165:241-245. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.05.015.
20. Gonçalves P, Valerio E, Correia C, de Almeida JM, Sampaio JP. 2011. Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6:e20739. http://dx.doi.org /10.1371/journal.pone.0020739.
21. Hittinger CT. 2013. Saccharomyces diversity and evolution: a budding model genus. Trends Genet. 29:309-317. http://dx.doi.org/10.1016/j.tig.2013.01.002.
22. Murata Y, Homma T, Kitagawa E, Momose Y, Sato MS, Odani M, Shimizu H, Hasegawa-Mizusawa M, Matsumoto R, Mizukami S, Fujita K, Parveen M, Komatsu Y, Iwahashi H. 2006. Genome-wide expression analysis of yeast response during exposure to 4°C. Extremophiles 10:117-128. http://dx.doi.org/10.1007/s00792-005-0480-1.
23. Schade B, Jansen G, Whiteway M, Entian KD, Thomas DY. 2004. Cold adaptation in budding yeast. Mol. Biol. Cell 15:5492-5502. http://dx.doi.org/10.1091/mbc.E04-03-0167.
24. Morano KA, Grant CM, Moye-Rowley WS. 2012. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190:1157-1195. http://dx.doi.org/10.1534/genetics.111.128033.
25. Hofmann S, Cherkasova V, Bankhead P, Bukau B, Stoecklin G. 2012. Translation suppression promotes stress granule formation and cell survival in response to cold shock. Mol. Biol. Cell 23:3786-3800. http://dx.doi.org/10.1091/mbc.E12-04-0296.
26. Aguilera J, Randez-Gil F, Prieto JA. 2007. Cold response in Saccharomyces cerevisiae: new functions for old mechanisms. FEMS Microbiol. Rev. 31:327-341. http://dx.doi.org/10.1111/j.1574-6976.2007.00066.x.
27. Leach MD, Cowen LE. 2013. Surviving the heat of the moment: a fungal pathogens perspective. PLoS Pathog. 9:e1003163. http://dx.doi.org/10.1371/journal.ppat.1003163.
28. + symporter Stl1p is essential for cold/near-freeze and freeze stress adaptation. A simple recipe with high biotechnological potential is given. Microb. Cell Fact. 9:82. http://dx.doi.org/10.1186/1475-2859-9-82.
29. Cruz AL, Verbon AJ, Geurink LJ, Verheijen PJ, Heijnen JJ, van Gulik WM. 2012. Use of sequential-batch fermentations to characterize the impact of mild hypothermic temperatures on the anaerobic stoichiometry and kinetics of Saccharomyces cerevisiae. Biotechnol. Bioeng. 109:1735-1744. http://dx.doi.org/10.1002/bit.24454.
30. Tai SL, Daran-Lapujade P, Luttik MAH, Walsh MC, Diderich JA, Krijger GC, van Gulik WM, Pronk JT, Daran JM. 2007. Control of the glycolytic flux in Saccharomyces cerevisiae grown at low temperature-a multi-level analysis in anaerobic chemostat cultures. J. Biol. Chem. 282: 10243-10251. http://dx.doi.org/10.1074/jbc.M610845200.
31. Tai SL, Daran-Lapujade P, Walsh MC, Pronk JT, Daran JM. 2007. Acclimation of Saccharomyces cerevisiae to low temperature: a chemostatbased transcriptome analysis. Mol. Biol. Cell 18:5100-5112. http://dx.doi.org/10.1091/mbc.E07-02-0131.
32. Cruz AL, Hebly M, Duong GH, Wahl SA, Pronk JT, Heijnen JJ, Daran-Lapujade P, van Gulik WM. 2012. Similar temperature dependencies of glycolytic enzymes: an evolutionary adaptation to temperature dynamics? BMC Syst. Biol. 6:151. http://dx.doi.org/10.1186/1752-0509-6-151.
33. Entian KD, Kötter P. 2007. Yeast genetic strain and plasmid collections, p 629-666. In Stansfield I, Stark MJR (ed), Yeast gene analysis, 2nd ed, vol. 36. Academic Press, San Diego, CA.
34. Nijkamp JF, van den Broek M, Datema E, de Kok S, Bosman L, Luttik MAH, Daran-Lapujade P, Vongsangnak W, Nielsen J, Heijne WH, Klaassen P, Paddon CJ, Platt D, Kötter P, van Ham RC, Reinders MJ, Pronk JT, de Ridder D, Daran JM. 2012. De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb. Cell Fact. 11:36. http://dx.doi.org/10.1186/1475-2859-11-36.
35. Verduyn C, Postma E, Scheffers WA, Van Dijken JP. 1990. Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J. Gen. Microbiol. 136:395-403. http://dx.doi.org/10.1099 /00221287-136-3-395.
36. Abbott DA, Suir E, Duong GH, de Hulster EAF, Pronk JT, van Maris AJA. 2009. Catalase overexpression reduces lactic acid-induced oxidative stress in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 75:2320-2325. http://dx.doi.org/10.1128/AEM.00009-09.
37. Boender LG, de Hulster EAF, van Maris AJA, Daran-Lapujade P, Pronk JT. 2009. Quantitative physiology of Saccharomyces cerevisiae at near-zero specific growth rates. Appl. Environ. Microbiol. 75:5607-5614. http://dx.doi.org/10.1128/AEM.00429-09.
38. Parrou JL, François J. 1997. A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal. Biochem. 248:186-188. http://dx.doi.org/10.1006/abio.1997.2138.
39. Porro D, Brambilla L, Alberghina L. 2003. Glucose metabolism and cell size in continuous cultures of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 229:165-171. http://dx.doi.org/10.1016/S0378-1097(03)00815-2.
40. Haase SB, Reed SI. 2002. Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 1:132-136. http://dx.doi.org/10.4161/cc.1.2.114.
41. Mendes F, Sieuwerts S, de Hulster EAF, Almering MJ, Luttik MAH, Pronk JT, Smid EJ, Bron PA, Daran-Lapujade P. 2013. Transcriptomebased characterization of interactions between Saccharomyces cerevisiae and Lactobacillus delbrueckii subsp. bulgaricus in lactose-grown chemostat cocultures. Appl. Environ. Microbiol. 79:5949-5961. http://dx.doi.org/10.1128/AEM.01115-13.
42. Boer VM, de Winde JH, Pronk JT, Piper MD. 2003. The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J. Biol. Chem. 278:3265-3274. http://dx.doi.org/10.1074/jbc.M209759200.
43. Boender LG, van Maris AJA, de Hulster EAF, Almering MJ, van der Klei IJ, Veenhuis M, de Winde JH, Pronk JT, Daran-Lapujade P. 2011. Cellular responses of Saccharomyces cerevisiae at near-zero growth rates: transcriptome analysis of anaerobic retentostat cultures. FEMS Yeast Res. 11:603-620. http://dx.doi.org/10.1111/j.1567-1364.2011.00750.x.
44. Storey JD, Xiao W, Leek JT, Tompkins RG, Davis RW. 2005. Significance analysis of time course microarray experiments. Proc. Natl. Acad. Sci. USA. 102:12837-12842. http://dx.doi.org/10.1073/pnas.0504609102.
45. Knijnenburg TA, de Winde JH, Daran JM, Daran-Lapujade P, Pronk JT, Reinders MJ, Wessels LF. 2007. Exploiting combinatorial cultivation conditions to infer transcriptional regulation. BMC Genomics 8:25. http: //dx.doi.org/10.1186/1471-2164-8-25.
46. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne JB, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA. 2004. Transcriptional regulatory code of a eukaryotic genome. Nature 431:99-104. http://dx.doi.org/10.1038/nature02800.
47. Bisschops MMM, Zwartjens P, Keuter SGF, Pronk JT, Daran-Lapujade P. 2014. To divide or not to divide: a key role of Rim15 in calorie-restricted yeast cultures. Biochim. Biophys. Acta 1843:1020-1030. http://dx.doi.org /10.1016/j.bbamcr.2014.01.026.
48. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ, Davis RW. 1998. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell 2:65-73. http://dx.doi.org/10.1016/S1097-2765(00)80114-8.
49. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9:3273-3297. http://dx.doi.org/10.1091/mbc.9.12.3273.
50. Kresnowati MT, van Winden WA, Almering MJ, ten Pierick A, Ras C, Knijnenburg TA, Daran-Lapujade P, Pronk JT, Heijnen JJ, Daran JM. 2006. When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol. Syst. Biol. 2:49. http://dx.doi.org/10.1038/msb4100083.
51. Van den Brink J, Daran-Lapujade P, Pronk JT, de Winde JH. 2008. New insights into the Saccharomyces cerevisiae fermentation switch: dynamic transcriptional response to anaerobicity and glucose-excess. BMC Genomics 9:100. http://dx.doi.org/10.1186/1471-2164-9-100.
52. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264. http://dx.doi.org/10.1093/biostatistics/4.2.249.
53. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193. http://dx.doi.org/10.1093/bioinformatics/19.2.185.
54. Ge YC, Dudoit S, Speed TP. 2003. Resampling-based multiple testing for microarray data analysis. Test 12:1-77. http://dx.doi.org/10.1007 /BF02595811.
55. Pearson K. 1901. On lines and planes of closest fit to systems of points in space. Philos. Mag. 2:559-572. http://dx.doi.org/10.1080/14786440109 462720.
56. Redon M, Borrull A, Lopez M, Salvado Z, Cordero R, Mas A, Guillamon JM, Rozes N. 2012. Effect of low temperature upon vitality of Saccharomyces cerevisiae phospholipid mutants. Yeast 29:443-452. http://dx.doi.org/10.1002/yea.2924.
57. Gancedo JM. 2008. The early steps of glucose signalling in yeast. FEMS Microbiol. Rev. 32:673-704. http://dx.doi.org/10.1111/j.1574-6976.2008.00117.x.
58. Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, Brown PO. 2001. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409:533-538. http://dx.doi.org/10.1038/35054095.
59. François J, Walther T, Parrou JL. 2012. Genetics and regulation of glycogen and trehalose metabolism in Saccharomyces cerevisiae, p 29-55. In Liu ZL (ed), Microbial stress tolerance for biofuels, 22nd ed. Springer, Berlin, Germany.
60. Panadero J, Pallotti C, Rodriguez-Vargas S, Randez-Gil F, Prieto JA. 2006. A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J. Biol. Chem. 281:4638-4645. http://dx.doi.org/10.1074/jbc.M512736200.
61. Sahara T, Goda T, Ohgiya S. 2002. Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. J. Biol. Chem. 277:50015-50021. http://dx.doi.org/10.1074/jbc.M209258200.
62. Frenz LM, Johnson AL, Johnston LH. 2001. Rme1, which controls CLN2 expression in Saccharomyces cerevisiae, is a nuclear protein that is cell cycle regulated. Mol. Genet. Genomics 266:374-384. http://dx.doi.org/10.1007 /s004380100515.
63. Knapp D, Bhoite L, Stillman DJ, Nasmyth K. 1996. The transcription factor Swi5 regulates expression of the cyclin kinase inhibitor p40SIC1. Mol. Cell. Biol. 16:5701-5707.
64. Monod J. 1949. The growth of bacterial cultures. Annu. Rev. Microbiol. 3:371-394. http://dx.doi.org/10.1146/annurev.mi.03.100149.002103.
65. Ter Linde JJ, Liang H, Davis RW, Steensma HY, Van Dijken JP, Pronk JT. 1999. Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae. J. Bacteriol. 181:7409-7413.
66. Henderson CM, Zeno WF, Lerno LA, Longo ML, Block DE. 2013. Fermentation temperature modulates phosphatidylethanolamine and phosphatidylinositol levels in the cell membrane of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 79:5345-5356. http://dx.doi.org/10.1128 /AEM.01144-13.
67. Tronchoni J, Rozes N, Querol A, Guillamon JM. 2012. Lipid composition of wine strains of Saccharomyces kudriavzevii and Saccharomyces cerevisiae grown at low temperature. Int. J. Food Microbiol. 155:191-198. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.02.004.
68. Kozak BU, van Rossum HM, Benjamin KR, Wu L, Daran JM, Pronk JT, van Maris AJA. 2014. Replacement of the Saccharomyces cerevisiae acetyl-CoA synthetases by alternative pathways for cytosolic acetyl-CoA synthesis. Metab. Eng. 21:46-59. http://dx.doi.org/10.1016/j.ymben.2013.11.005.
69. Corcoles-Saez I, Ballester-Tomas L, de la Torre-Ruiz MA, Prieto JA, Randez-Gil F. 2012. Low temperature highlights the functional role of the cell wall integrity pathway in the regulation of growth in Saccharomyces cerevisiae. Biochem. J. 446:477-488. http://dx.doi.org/10.1042 /BJ20120634.
70. Kuismanen E, Saraste J. 1989. Low temperature-induced transport blocks as tools to manipulate membrane traffic. Methods Cell Biol. 32: 257-274. http://dx.doi.org/10.1016/S0091-679X(08)61174-7.
71. Martinez-Alonso E, Ballesta J, Martinez-Menarguez JA. 2007. Lowtemperature-induced Golgi tubules are transient membranes enriched in molecules regulating intra-Golgi transport. Traffic 8:359-368. http://dx.doi.org/10.1111/j.1600-0854.2006.00533.x.
72. Hanson PK, Grant AM, Nichols JW. 2002. NBD-labeled phosphatidylcholine enters the yeast vacuole via the pre-vacuolar compartment. J. Cell Sci. 115:2725-2733. http://jcs.biologists.org/content/115/13/2725.long.
73. Abe F, Minegishi H. 2008. Global screening of genes essential for growth in high-pressure and cold environments: searching for basic adaptive strategies using a yeast deletion library. Genetics 178:851-872. http://dx.doi.org/10.1534/genetics.107.083063.
74. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347-4368. http://dx.doi.org/10.1128/MCB.21.13.4347-4368.2001.
75. Beltran G, Rozes N, Mas A, Guillamon JM. 2007. Effect of lowtemperature fermentation on yeast nitrogen metabolism. World J. Microbiol. Biotechnol. 23:809-815. http://dx.doi.org/10.1007/s11274-006-9302-6.
76. Eelderink-Chen Z, Mazzotta G, Sturre M, Bosman J, Roenneberg T, Merrow M. 2010. A circadian clock in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 107:2043-2047. http://dx.doi.org/10.1073/pnas.0907902107.
77. Futcher B. 2006. Metabolic cycle, cell cycle, and the finishing kick to Start. Genome Biol. 7:107. http://dx.doi.org/10.1186/gb-2006-7-4-107.
78. Tu BP, Kudlicki A, Rowicka M, McKnight SL. 2005. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310:1152-1158. http://dx.doi.org/10.1126/science.1120499.
79. Klevecz RR, Bolen J, Forrest G, Murray DB. 2004. A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc. Natl. Acad. Sci. USA. 101:1200-1205. http://dx.doi.org/10.1073/pnas.0306490101.
80. Silverman SJ, Petti AA, Slavov N, Parsons L, Briehof R, Thiberge SY, Zenklusen D, Gandhi SJ, Larson DR, Singer RH, Botstein D. 2010. Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate. Proc. Natl. Acad. Sci. USA. 107:6946-6951. http://dx.doi.org/10.1073/pnas.1002422107.
81. Vanoni M, Vai M, Frascotti G. 1984. Effects of temperature on the yeast cell cycle analyzed by flow cytometry. Cytometry 5:530-533. http://dx.doi.org/10.1002/cyto.990050515.
82. Sillje HHW, ter Schure EG, Rommens AJM, Huls PG, Woldringh CL, Verkleij AJ, Boonstra J, Verrips CT. 1997. Effects of different carbon fluxes on G1 phase duration, cyclin expression, and reserve carbohydrate metabolism in Saccharomyces cerevisiae. J. Bacteriol. 179:6560-6565.
83. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D. 2008. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol. Biol. Cell 19:352-367. http://dx.doi.org/10.1091/mbc.E07-08-0779.
84. Hazelwood LA, Walsh MC, Luttik MAH, Daran-Lapujade P, Pronk JT, Daran JM. 2009. Identity of the growth-limiting nutrient strongly affects storage carbohydrate accumulation in anaerobic chemostat cultures of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 75:6876-6885. http: //dx.doi.org/10.1128/AEM.01464-09.
85. Wilson WA, Roach PJ, Montero M, Baroja-Fernandez E, Munoz FJ, Eydallin G, Viale AM, Pozueta-Romero J. 2010. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol. Rev. 34:952-985. http: //dx.doi.org/10.1111/j.1574-6976.2010.00220.x.
86. Mowll JL, Gadd GM. 1983. Zinc uptake and toxicity in the yeasts Sporobolomyces roseus and Saccharomyces cerevisiae. J. Gen. Microbiol. 129:3421-3425.
87. de Nicola R, Hazelwood LA, de Hulster EAF, Walsh MC, Knijnenburg TA, Reinders MJ, Walker GM, Pronk JT, Daran JM, Daran-Lapujade P. 2007. Physiological and transcriptional responses of Saccharomyces cerevisiae to zinc limitation in chemostat cultures. Appl. Environ. Microbiol. 73:7680-7692. http://dx.doi.org/10.1128/AEM.01445-07.
88. Kasemets K, Nisamedtinov I, Laht TM, Abner K, Paalme T. 2007. Growth characteristics of Saccharomyces cerevisiae S288C in changing environmental conditions: auxo-accelerostat study. Antonie Van Leeuwenhoek 92:109-128. http://dx.doi.org/10.1007/s10482-007-9141-y.