Cell Cycle Synchrony of Propagated and Recycled Lager Yeast and its Impact on Lag Phase in Fermenter

Literature Cited

• Anderson, R. G., and Kirsop, B. H. Oxygen as a regulator of ester accumulation during the fermentation of worts of high specific gravity. J. Inst. Brew. 81:111–115, 1975.
   Web of Science ®Google Scholar
• Anderson, R. G., and Kirsop, B. H. Quantitative aspects of the control by oxygenation of acetate ester formation of worts of high specific gravity. J. Inst. Brew. 81:296–301, 1975.
   Web of Science ®Google Scholar
• Andreasen, A., and Stier, T. Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J. Cell. Comp. Physiol. 41:23–36, 1953.
   PubMedGoogle Scholar
• Andreasen, A., and Stier, T. Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in defined medium,. J. Cell. Comp. Physiol. 43:271–281, 1954.
   PubMedGoogle Scholar
• Aries, V., and Kirsop, B. H. Sterol synthesis in relation to growth and fermentation by brewing inoculated at different concentrations. J. Inst. Brew. 83:220–223, 1977.
   Web of Science ®Google Scholar
• Barford, J. P., and Hall, R. J. Estimation of the length of cell cycle phases from asynchronous cultures of Saccharomyces cerevisiae. Exp. Cell Res. 102:276–284, 1976.
   Web of Science ®Google Scholar
• Blomberg, A. Osmoresponsive proteins and functional assessment strategies in Saccharomyces cerevisiae. Electrophoresis 18:1429–1440, 1997.
   Web of Science ®Google Scholar
• Bloomfield, D. K., and Bloch, K. The formation of delta 9-unsaturated fatty acids. J. Biol. Chem. 235:337–345, 1960.
   PubMed Web of Science ®Google Scholar
• Boulton, C. A., and Quain, D. E. Yeast, oxygen and the control of brewery fermentation. Proc. Congr. Eur. Brew. Conv. 21:401–408, 1987.
   Google Scholar
• Boulton, C. A. Yeast distribution in cylindroconical vessels, new insights into fermentation performance and management. Proc. Congr. Eur. Brew. Conv. Venice, 2007.
   Google Scholar
• Boulton, C. A. Yeast management and the control of brewery fermentations. Brew. Guard. 120:25–29, 1991.
   Google Scholar
• Brauer, M. J., Huttenhower, C., Airoldi, E. M., Rosenstein, R., Matese, J. C., Gresham, D., Boer, V. M., Troyanskaya, O. G., and Botstein, D. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol. Biol. Cell 19:352–367, 2008.
   PubMed Web of Science ®Google Scholar
• Brejning, J., and Jespersen, L. Protein expression during lag phase and growth initiation in Saccharomyces cerevisiae. Int. J. Food Microbiol. 75:27–38, 2002.
   Web of Science ®Google Scholar
• Briggs, D. E., Boulton, C. A., Brookes, P. A., and Rogers, S. Brewing: Science and Practice. Woodhead, Cambridge, 2004.
   Google Scholar
• Cahill, G., Murray, D. M., Walsh, P. K., and Donnelly, D. Effect of the concentration of propagation wort on yeast cell volume and fermentation performance. J. Am. Soc. Brew. Chem. 58:14–20, 2000.
   Web of Science ®Google Scholar
• Carroll, A. S., and O'Shea, E. K. Pho85 and signaling environmental conditions. Trends Biochem. Sci. 27:87–93, 2002.
   PubMed Web of Science ®Google Scholar
• Casey, G. P., Magnus, C. A., and Ingledew, W. M. High-gravity brewing—Effects of nutrition on yeast composition, fermentative ability and alcohol production. Appl. Environ. Microbiol. 48:639–646, 1984.
   PubMed Web of Science ®Google Scholar
• Cross, F. R. Starting the cell cycle: What's the point? Curr. Opin. Cell. Biol. 7:790–797, 1995.
   PubMed Web of Science ®Google Scholar
• Cvrckova, F., and Nasmyth, K. Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J. 12:5277–5286, 1993.
   PubMed Web of Science ®Google Scholar
• D'Amore, T. Improving yeast fermentation performance. J. Inst. Brew. 98:375–382, 1992.
   Web of Science ®Google Scholar
• Dombek, K. M., and Ingram, L. O. Determination of the intracellular concentration of ethanol in Saccharomyces cerevisiae during fermentation. Appl. Environ. Microbiol. 51:197–200, 1986.
   PubMed Web of Science ®Google Scholar
• Dombek, K. M., and Ingram, L. O. Magnesium limitation and its role in apparent toxicity of ethanol during yeast fermentation. Appl. Environ. Microbiol. 52:975–981, 1986.
   PubMed Web of Science ®Google Scholar
• Edelen, C. L., Miller, J. L., and Patino, H. Effects of pitch rate on fermentation performance and beer quality. Tech. Q. Master Brew. Assoc. Am. 33:30–32, 1996.
   Google Scholar
• Erten, H., Tanguler, H., and Cakiroz, H. The effect of pitching rate on fermentation and flavour compounds in high gravity brewing J. Inst. Brew. 113:75–79, 2007.
   Web of Science ®Google Scholar
• Futcher, B. Metabolic cycle, cell cycle, and the finishing kick to Start. Genome Biol. 7:107, 2006.
   PubMed Web of Science ®Google Scholar
• Gibson, B. R., Lawrence, S. J., Boulton, C. A., Box, W. G., Graham, N. S., Linforth, R. S. T., and Smart, K. A. Genomic analysis of yeast stress responses during industrial propagation and fermentation Proc. Congr. Eur. Brew. Conv. 31, 2007.
   Google Scholar
• Gibson, B. R., Lawrence, S. J., Leclaire, J. P., Powell, C. D., and Smart, K. A. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol. Rev. 31:535–569, 2007.
   PubMed Web of Science ®Google Scholar
• Granot, D., and Snyder, M. Glucose induces cAMP-independent growth-related changes in stationary-phase cells of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88:5724–5728, 1991.
   PubMed Web of Science ®Google Scholar
• Gray, J. V., Petsko, G. A., Johnston, G. C., Ringe, D., Singer, R. A., and Werner-Washburne, M. “Sleeping beauty”: Quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 68:187–206, 2004.
   PubMed Web of Science ®Google Scholar
• Guo, J., Bryan, B. A., and Polymenis, M. Nutrient-specific effects in the coordination of cell growth with cell division in continuous cultures of Saccharomyces cerevisiae. Arch. Microbiol. 182:326–330, 2004.
   Web of Science ®Google Scholar
• Haase, S. B., and Daniel, J. L. Flow cytometric analysis of DNA content in budding yeast. Methods Enzymol. 283:322, 1997.
   PubMed Web of Science ®Google Scholar
• Haase, S. B., and Reed, S. I. Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 1:132–136, 2002.
   PubMed Web of Science ®Google Scholar
• Hartwell, L. H. Saccharomyces cerevisiae cell cycle. Bacteriol. Rev. 38:164–198, 1974.
   PubMedGoogle Scholar
• Hartwell, L. H., and Unger, M. W. Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J. Cell Biol. 75:422–435, 1977.
   PubMed Web of Science ®Google Scholar
• Haukeli, A. D., and Lie, S. Yeast growth and metabolic changes during brewery fermentation. Proc. Congr. Eur. Brew. Conv. 17:461–473, 1979.
   Google Scholar
• Hutter, K. J. Flow cytometry—A new tool for direct control of fermentation processes. J. Inst. Brew. 108:48–51, 2002.
   Web of Science ®Google Scholar
• Jenkins, C. L., Kennedy, A. I., Hodgson, J. A., Thurston, P., and Smart, K. A. Impact of serial repitching on lager brewing yeast quality. J. Am. Soc. Brew. Chem. 61:1–9, 2003.
   Web of Science ®Google Scholar
• Jenkins, C. L., Lawrence, S. J., Kennedy, A. I., Thurston, P., Hodgson, J. A., and Smart, K. A. Incidence and formation of petite mutants in lager brewing yeast Saccharomyces cerevisiae (syn. S. pastorianus) populations. J. Am. Soc. Brew. Chem. 67:72–80, 2009.
   Web of Science ®Google Scholar
• Johnston, G. C. Cell size and budding during starvation of the yeast Saccharomyces cerevisiae. J. Bacteriol. 132:738–739, 1977.
   PubMed Web of Science ®Google Scholar
• Johnston, G. C., Pringle, J. R., and Hartwell, L. H. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp. Cell Res. 105:79–98, 1977.
   PubMed Web of Science ®Google Scholar
• Jones, H. L. Yeast propagation—Past, present and future. Brew. Guard. 126:24–27, 1997.
   Google Scholar
• Jorgensen, P., Nishikawa, J. L., Breitkreutz, B. J., and Tyers, M. Systematic identification of pathways that couple cell growth and division in yeast. Science 297:395–400, 2002.
   PubMed Web of Science ®Google Scholar
• Jorgensen, P., and Tyers, M. How cells coordinate growth and division. Curr. Biol. 14:R1014–1027, 2004.
   PubMed Web of Science ®Google Scholar
• Kalmokoff, M. L., and Ingledew, W. M. Evaluation of ethanol tolerance in selected Saccharomyces strains. J. Am. Soc. Brew. Chem. 43:189–196, 1985.
   Google Scholar
• Klein, H. P. Synthesis of lipids in resting cells of Saccharomyces cerevisiae. J. Bacteriol. 69:620–627, 1955.
   PubMedGoogle Scholar
• Knatchbull, F. B., and Slaughter, J. C. The effect of low CO2 pressures on the absorption of amino-acids and production of flavor-active volatiles by yeast. J. Inst. Brew. 93:420–424, 1987.
   Web of Science ®Google Scholar
• Laabs, T. L., Markwardt, D. D., Slattery, M. G., Newcomb, L. L., Stillman, D. J., and Heideman, W. ACE2 is required for daughter cell-specific G1 delay in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100:10275–10280, 2003.
   PubMed Web of Science ®Google Scholar
• Li, F. N., and Johnston, M. Grr1 of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skp1: Coupling glucose sensing to gene expression and the cell cycle. EMBO J. 16:5629–5638, 1997.
   PubMed Web of Science ®Google Scholar
• Ma, P., Goncalves, T., Maretzek, A., Dias, M. C., and Thevelein, J. M. The lag phase rather than the exponential-growth phase on glucose is associated with a higher cAMP level in wild-type and cAPK-attenuated strains of the yeast Saccharomyces cerevisiae. Microbiology 143:3451–3459, 1997.
   Web of Science ®Google Scholar
• McCaig, R., and Bendiak, D. Yeast handling studies. I. Agitation of stored pitching yeast. J. Am. Soc. Brew. Chem. 43:119–122, 1985.
   Google Scholar
• McCaig, R., and Bendiak, D. S. Yeast handling studies. II. temperature of storage of pitching yeast. J. Am. Soc. Brew. Chem. 43:119–122, 1985.
   Google Scholar
• Miller, K. J., Gibson, B. R., Lawrence, S. J., Boulton, C. A., and Smart, K. A. Towards a consistent lag phase in fermenter: Predictive biomarkers of brewery yeast performance. Proc. Congr. Eur. Brew. Conv. 31, 2007.
   Google Scholar
• Moonjai, N., Verstrepen, K. J., Delvaux, F. R., Derdelinckx, G., and Verachtert, H. The effects of linoleic acid supplementation of cropped yeast on its subsequent fermentation performance and acetate ester synthesis. J. Inst. Brew. 108:227–235, 2002.
   Web of Science ®Google Scholar
• Muller, D., Exler, S., Aguilera-Vazquez, L., Guerrero-Martin, E., and Reuss, M. Cyclic AMP mediates the cell cycle dynamics of energy metabolism in Saccharomyces cerevisiae. Yeast 20:351–367, 2003.
   PubMed Web of Science ®Google Scholar
• Nagodawithana, T. W., and Steinkraus, K. H. Influence of the rate of ethanol production and accumulation on the viability of Saccharomyces cerevisiae in “rapid fermentation.” Appl. Environ. Microbiol. 31:158–162, 1976.
   PubMed Web of Science ®Google Scholar
• Neufeld, T. P., and Edgar, B. A. Connections between growth and the cell cycle. Curr. Opin. Cell. Biol. 10:784–790, 1998.
   PubMed Web of Science ®Google Scholar
• Newcomb, L. L., Diderich, J. A., Slattery, M. G., and Heideman, W. Glucose regulation of Saccharomyces cerevisiae cell cycle genes. Eukaryot. Cell 2:143–149, 2003.
   PubMedGoogle Scholar
• Norton, J. S., and Krauss, R. W. The inhibition of cell division in Saccharomyces cerevisiae (Meyen) by carbon dioxide. Plant Cell Physiol. 13:139–149, 1972.
   Web of Science ®Google Scholar
• O'Connor-Cox, E. S. C. Improving yeast handling in the brewery. Part 2: Yeast collection. Brew. Guard. 122:22–34, 1998.
   Google Scholar
• Oliver, S. Guilt-by-association goes global. Nature 403:601–603, 2000.
   PubMed Web of Science ®Google Scholar
• Orlando, D. A., Lin, C. Y., Bernard, A., Iversen, E. S., Hartemink, A. J., and Haase, S. B. A probabilistic model for cell cycle distributions in synchrony experiments. Cell Cycle 6:478–488, 2007.
   PubMed Web of Science ®Google Scholar
• Parks, L. W. Metabolism of sterols in yeast. CRC Crit. Rev. Microbiol. 6:301–341, 1978.
   PubMed Web of Science ®Google Scholar
• Pierce, J. S. Measurement of yeast viability. J. Inst. Brew. 76:442–443, 1970.
   Web of Science ®Google Scholar
• Plesset, J., Ludwig, J. R., Cox, B. S., and McLaughlin, C. S. Effect of cell cycle position on thermotolerance in Saccharomyces cerevisiae. J. Bacteriol. 169:779–784, 1987.
   PubMed Web of Science ®Google Scholar
• Powell, C. D., and Diacetis, A. N. Long-term serial repitching and the genetic and phenotypic stability of brewer's yeast. J. Inst. Brew. 113:67–74, 2007.
   Web of Science ®Google Scholar
• Powell, C. D., Quain, D. E., and Smart, K. A. The impact of brewing yeast cell age on fermentation performance, attenuation and flocculation. FEMS Yeast Res. 3:149–157, 2003.
   Web of Science ®Google Scholar
• Pringle, J. R., and Hartwell, L. H. The Saccharomyces cell cycle. In: The Molecular Biology of the Yeast Saccharomyces cerevisiae: Life Cycle and Inheritance. J. N. Strathen, E. W. Jones, and J. R. Broach, eds. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1981.
   Google Scholar
• Quain, D. E. The determination of glycogen in yeasts. J. Inst. Brew. 87:289–291, 1981.
   Web of Science ®Google Scholar
• Quain, D. E. Studies on yeast physiology—Impact on fermentation performance and product quality. J. Inst. Brew. 95:315–323, 1988.
   Web of Science ®Google Scholar
• Rogers, P. J., and Stewart, P. R. Mitochondrial and peroxisomal contributions to the energy metabolism of Saccharomyces cerevisiae in continuous culture. J. Gen. Microbiol. 79:205–217, 1973.
   Google Scholar
• Rupes, I. Checking cell size in yeast. Trends Genet. 18:479–485, 2002.
   PubMed Web of Science ®Google Scholar
• Sall, C. J., Seipp, J. F., and Pringle, A.T. Changes in brewer's yeast during storage and the effect of these changes on subsequent fermentation performance. J. Am. Soc. Brew. Chem. 46:23–25, 1988.
   Google Scholar
• Schneider, B. L., Zhang, J., Markwardt, J., Tokiwa, G., Volpe, T., Honey, S., and Futcher, B. Growth rate and cell size modulate the synthesis of, and requirement for, G1-phase cyclins at start. Mol. Cell. Biol. 24:10802–10813, 2004.
   PubMed Web of Science ®Google Scholar
• Schwob, E., and Nasmyth, K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Gene Dev. 7:1160–1175, 1993.
   PubMed Web of Science ®Google Scholar
• Sillje, H. H., Paalman, J. W., ter Schure, E. G., Olsthoorn, S. Q., Verkleij, A. J., Boonstra, J., and Verrips, C. T. Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae. J. Bacteriol. 181:396–400, 1999.
   Web of Science ®Google Scholar
• Sillje, H. H., ter Schure, E. G., Rommens, A. J., Huls, P. G., Woldringh, C. L., Verkleij, A. J., Boonstra, J., and Verrips, C. T. Effects of different carbon fluxes on G1 phase duration, cyclin expression, and reserve carbohydrate metabolism in Saccharomyces cerevisiae. J. Bacteriol. 179:6560–6565, 1997.
   PubMed Web of Science ®Google Scholar
• Slater, M. L., Sharrow, S. O., and Gart, J. J. Cell cycle of Saccharomyces cerevisiae in populations growing at different rates. Proc. Natl. Acad. Sci. USA 74:3850–3854, 1977.
   PubMed Web of Science ®Google Scholar
• Slaughter, J. C., and McKernan, G. The influence of pantothenate concentration and inoculum size on the fermentation of a defined medium by Saccharomyces cerevisiae. J. Inst. Brew. 94:14–18, 1988.
   Web of Science ®Google Scholar
• Smart, K. A., and Whisker, S. Effect of serial repitching on the fermentation properties and condition of brewing yeast. J. Am. Soc. Brew. Chem. 54:41–44, 1996.
   Web of Science ®Google Scholar
• Stewart, G. G., and Russell, I. Fermentation—The “black box” of the brewing process. Tech. Q. Master Brew. Assoc. Am. 30:159–168, 1993.
   Google Scholar
• Suihko, M. L., Vilpola, A., and Linko, M. Pitching rate in high gravity brewing. J. Inst. Brew. 99:341–346, 1993.
   Web of Science ®Google Scholar
• van Aelst, L., Jans, A. W., and Thevelein, J. M. Involvement of the CDC25 gene product in the signal transmission pathway of the glucose-induced RAS-mediated cAMP signal in the yeast Saccharomyces cerevisiae. J. Gen. Microbiol. 137:341–349, 1991.
   PubMedGoogle Scholar
• Van Bogelen, R. A., Schiller, E. E., Thomas, J. D., and Neidhardt, F. C. Diagnosis of cellular states of microbial organisms using proteomics. Electrophoresis 20:2149–2159, 1999.
   PubMed Web of Science ®Google Scholar
• Van Uden, N. Temperature profiles of yeasts. Adv. Microb. Physiol. 25:195–251, 1984.
   PubMed Web of Science ®Google Scholar
• Verbelen, P. J., Dekoninck, T. M., Saerens, S. M., Van Mulders, S. E., Thevelein, J. M., and Delvaux, F. R. Impact of pitching rate on yeast fermentation performance and beer flavour. Appl. Microbiol. Biotechnol. 82:155–167, 2009.
   Web of Science ®Google Scholar
• Verbelen, P. J., Saerens, S. M., Van Mulders, S. E., Delvaux, F., and Delvaux, F. R. The role of oxygen in yeast metabolism during high cell density brewery fermentations. Appl. Microbiol. Biotechnol. 82:1143–1156, 2009.
   Web of Science ®Google Scholar
• Werner-Washburne, M., Braun, E., Johnston, G. C., and Singer, R. A. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol. Rev. 57:383–401, 1993.
   Google Scholar
• Wheals, A. E. Biology of the cell cycle in yeasts. In: The Yeasts. A. H. Rose and J. S. Harrison, eds. Academic Press, London. Pp. 283–390, 1987.
   Google Scholar