Sustainability of industrial yeast serial repitching practice studied by gene expression and correlation analysis

Achilles, 2007, Isolation of intact RNA from cytometrically sorted Saccharomyces cerevisiae for the analysis of intrapopulation diversity of gene expression, Nat. Protoc., 2, 2203, 10.1038/nprot.2007.322 Ackermann, 2001, Genes targeted by protein kinase CK2: a genome-wide expression array analysis in yeast, Mol. Cell. Biochem., 227, 59, 10.1023/A:1013104705100 Alexandre, 2001, Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae, FEBS Lett., 498, 98, 10.1016/S0014-5793(01)02503-0 Anraku, 1991, Cell cycle control by calcium and calmodulin in Saccharomyces cerevisiae, Biochim. Biophys. Acta—Mol. Cell Res., 1093, 169, 10.1016/0167-4889(91)90119-I Archambault, 1993, Genetics of eukaryotic RNA polymerases I, II, and III, Microbiol. Rev., 57, 703, 10.1128/MMBR.57.3.703-724.1993 Attfield, 1997, Stress tolerance: the key to effective strains of industrial baker's yeast, Nat. Biotech., 15, 1351, 10.1038/nbt1297-1351 Back, 2008 Bandara, 1998, Involvement of the Saccharomyces cerevisiae UTH1 gene in the oxidative-stress response, Curr. Genet., 34, 259, 10.1007/s002940050395 Beckman, 1998, The free radical theory of aging matures, Physiol. Rev., 78, 547, 10.1152/physrev.1998.78.2.547 Benaroudj, 2001, Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals, J. Biol. Chem., 276, 24261, 10.1074/jbc.M101487200 Bermingham-McDonogh, 1988, The copper, zinc-superoxide dismutase gene of Saccharomyces cerevisiae: cloning, sequencing, and biological activity, PNAS, 85, 4789, 10.1073/pnas.85.13.4789 Boulton, 1991, Developments in brewery fermentation, Biotechnol. Genet. Eng. Rev., 9, 127 Brands, 2002, Function of a plant stress-induced gene, HVA22: Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic, Plant Physiol., 130, 1121, 10.1104/pp.007716 Brewster, 1993, An osmosensing signal transduction pathway in yeast, Science, 259, 1760, 10.1126/science.7681220 Bustin, 2009, The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 55, 611, 10.1373/clinchem.2008.112797 Calero, 2001, Yop1p, the yeast homolog of the polyposis locus protein 1, interacts with Yip1p and negatively regulates cell growth, J. Biol. Chem., 276, 12100, 10.1074/jbc.M008439200 Camougrand, 2003, The product of the UTH1 gene, required for Bax-induced cell death in yeast, is involved in the response to rapamycin, Mol. Microbiol., 47, 495, 10.1046/j.1365-2958.2003.03311.x Cheong, 2008, Optimal conditions for propagation in bottom and top brewing yeast strains, Food Sci. Biotechnol., 17, 739 Ciriacy, 1975, Genetics of alcohol dehydrogenase in Saccharomyces cerevisiae. II. Two loci controlling synthesis of the glucose-repressible ADH II, Mol. Gen. Genet., 138, 157, 10.1007/BF02428119 Cueva, 1989, Yeast vacuolar aminopeptidase yscI: isolation and regulation of the APE1 (LAP4) structural gene, FEBS Lett., 259, 125, 10.1016/0014-5793(89)81510-8 de Bruin, 2006, Constraining G1-specific transcription to late G1 phase: the MBF-associated corepressor Nrm1 acts via negative feedback, Mol. Cell, 23, 483, 10.1016/j.molcel.2006.06.025 de Groot, 2007, Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals posttranscriptional regulation of key cellular processes, Microbiology, 153, 3864, 10.1099/mic.0.2007/009969-0 De Hertogh, 2002, Phylogenetic classification of transporters and other membrane proteins from Saccharomyces cerevisiae, Funct. Integr. Genomics, 2, 154, 10.1007/s10142-002-0060-8 DeRisi, 1997, Exploring the metabolic and genetic control of gene expression on a genomic scale, Science, 278, 680, 10.1126/science.278.5338.680 1999 Easlon, 2008, The malate–aspartate NADH shuttle components are novel metabolic longevity regulators required for calorie restriction-mediated life span extension in yeast, Gene Dev., 22, 931, 10.1101/gad.1648308 Eisen, 1998, Cluster analysis and display of genome-wide expression patterns, PNAS, 95, 14863, 10.1073/pnas.95.25.14863 Eisenberg, 2009, Induction of autophagy by spermidine promotes longevity, Nat. Cell Biol., 11, 1305, 10.1038/ncb1975 Fabrizio, 2003, The chronological life span of Saccharomyces cerevisiae, Aging Cell, 2, 73, 10.1046/j.1474-9728.2003.00033.x Fabrizio, 2004, Chronological aging-independent replicative life span regulation by Msn2/Msn4 and Sod2 in Saccharomyces cerevisiae, FEBS Lett., 557, 136, 10.1016/S0014-5793(03)01462-5 Fabrizio, 2001, Regulation of longevity and stress resistance by Sch9 in yeast, Science, 292, 288, 10.1126/science.1059497 Fitch, 1992, Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae, Mol. Biol. Cell, 3, 805, 10.1091/mbc.3.7.805 Funakoshi, 1997, Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae, Gene, 192, 207, 10.1016/S0378-1119(97)00031-0 Gasch, 2000, Genomic expression programs in the response of yeast cells to environmental changes, Mol. Biol. Cell, 11, 4241, 10.1091/mbc.11.12.4241 Gasch, 2002, The genomics of yeast responses to environmental stress and starvation, Funct. Integr. Genomic, 2, 181, 10.1007/s10142-002-0058-2 Gibson, 2008, Carbohydrate utilization and the lager yeast transcriptome during brewery fermentation, Yeast, 25, 549, 10.1002/yea.1609 Gibson, 2008, The oxidative stress response of a lager brewing yeast strain during industrial propagation and fermentation, FEMS Yeast Res., 8, 574, 10.1111/j.1567-1364.2008.00371.x Gibson, 2007, Yeast responses to stresses associated with industrial brewery handling, FEMS Microbiol. Rev., 31, 535, 10.1111/j.1574-6976.2007.00076.x Greenbaum, 2003, Comparing protein abundance and mRNA expression levels on a genomic scale, Genome Biol., 4, 117, 10.1186/gb-2003-4-9-117 Greetham, 2009, Antioxidant activity of the yeast mitochondrial one-Cys peroxiredoxin is dependent on thioredoxin reductase and glutathione in vivo, Mol. Cell Biol., 29, 3229, 10.1128/MCB.01918-08 Günther, 2012, Correlation of community dynamics and process parameters as a tool for the prediction of the stability of wastewater treatment, Environ. Sci. Technol., 46, 84, 10.1021/es2010682 Gygi, 1999, Correlation between protein and mRNA abundance in yeast, Mol. Cell Biol., 19, 1720, 10.1128/MCB.19.3.1720 Hammer, 2001, PAST: paleontological statistics software package for education and data analysis, Palaeontol. Electron., 4, 9 Heine, 2009, Prediction of flocculation ability of brewing yeast inoculates by flow cytometry, proteome analysis, and mRNA profiling, Cytometry, 75A, 140, 10.1002/cyto.a.20661 Herdeiro, 2006, Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress, Biochim. Biophys. Acta—Gen. Subj., 1760, 340, 10.1016/j.bbagen.2006.01.010 Horinouchi, 2010, Genome-wide expression analysis of Saccharomyces pastorianus orthologous genes using oligonucleotide microarrays, J. Biosci. Bioeng., 110, 602, 10.1016/j.jbiosc.2010.05.011 Ismail, 2013, Gene expression cross-profiling in genetically modified industrial Saccharomyces cerevisiae strains during high-temperature ethanol production from xylose, J. Biotech., 163, 50, 10.1016/j.jbiotec.2012.10.017 James, 2003, Transcription profile of brewery yeast under fermentation conditions, J. Appl. Microbiol., 94, 432, 10.1046/j.1365-2672.2003.01849.x Kabeya, 2005, Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy, Mol. Biol. Cell, 16, 2544, 10.1091/mbc.E04-08-0669 Kaeberlein, 2004, Saccharomyces cerevisiae SSD1-V confers longevity by a Sir2p-independent mechanism, Genetics, 166, 1661, 10.1534/genetics.166.4.1661 Kaeberlein, 2005, Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients, Science, 310, 1193, 10.1126/science.1115535 Kahl, 2003, Regulation of cell cycle progression by calcium/calmodulin-dependent pathways, Endocr. Rev., 24, 719, 10.1210/er.2003-0008 Kobayashi, 1998, Region of Flo1 proteins responsible for sugar recognition, J. Bacteriol., 180, 6503, 10.1128/JB.180.24.6503-6510.1998 Kobi, 2004, Two-dimensional protein map of an ale-brewing yeast strain: proteome dynamics during fermentation, FEMS Yeast Res., 5, 213, 10.1016/j.femsyr.2004.07.004 Krogan, 2003, The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation, Mol. Cell, 11, 721, 10.1016/S1097-2765(03)00091-1 Lawson, 1991, Disruption and mutagenesis of the Saccharomyces cerevisiae PDX1 gene encoding the protein X component of the pyruvate dehydrogenase complex, Biochemistry, 30, 2834, 10.1021/bi00225a015 Lense, 1996, 16 Levine, 2011, Autophagy in immunity and inflammation, Nature, 469, 323, 10.1038/nature09782 Li, 2009, Budding yeast SSD1-V regulates transcript levels of many longevity genes and extends chronological life span in purified quiescent cells, Mol. Biol. Cell, 20, 3851, 10.1091/mbc.E09-04-0347 Libkind, 2011, Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast, PNAS, 108, 14539, 10.1073/pnas.1105430108 Longo, 1996, Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae, J. Biol. Chem., 271, 12275, 10.1074/jbc.271.21.12275 Lorenz, 1991, Involvement of heme components in sterol metabolism of Saccharomyces cerevisiae, Lipids, 26, 598, 10.1007/BF02536423 Maier, 2009, Correlation of mRNA and protein in complex biological samples, FEBS Lett., 583, 3966, 10.1016/j.febslet.2009.10.036 Mason, 2000, Alcohol acetyltransferases and the significance of ester synthesis in yeast, Yeast, 16, 1287, 10.1002/1097-0061(200010)16:14<1287::AID-YEA613>3.0.CO;2-I Masumoto, 2002, S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast, Nature, 415, 651, 10.1038/nature713 Mesecke, 2008, A novel group of glutaredoxins in the cis-golgi critical for oxidative stress resistance, Mol. Biol. Cell, 19, 2673, 10.1091/mbc.E07-09-0896 Minato, 2009, Expression profiling of the bottom fermenting yeast Saccharomyces pastorianus orthologous genes using oligonucleotide microarrays, Yeast, 26, 147, 10.1002/yea.1654 Mortimer, 1959, Life span of individual yeast cells, Nature, 183, 1751, 10.1038/1831751a0 Müller, 1997, Dynamics of yeast cell states during proliferation and non proliferation periods in a brewing reactor monitored by multidimensional flow cytometry, Bioproc. Biosyst. Eng., 17, 287, 10.1007/s004490050387 Narziß, 1995, 6 Nijtmans, 2000, Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins, EMBO J., 19, 2444, 10.1093/emboj/19.11.2444 Oksanen, 2011, Vegan: Community Ecology Package, 0 Ozcan, 1999, Function and regulation of yeast hexose transporters, Microbiol. Mol. Biol. Res., 63, 554, 10.1128/MMBR.63.3.554-569.1999 Padmanabha, 1990, Isolation, sequencing, and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae, Mol. Cell Biol., 10, 4089, 10.1128/MCB.10.8.4089 Paravicini, 1992, The yeast FBP26 gene codes for a fructose-2,6-bisphosphatase, Biochemistry—US, 31, 7126, 10.1021/bi00146a014 Parrou, 1997, Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose, Microbiology (Reading, Engl.), 143, 1891, 10.1099/00221287-143-6-1891 Pedrajas, 2000, Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity, J. Biol. Chem., 275, 16296, 10.1074/jbc.275.21.16296 Piper, 2002, Reproducibility of oligonucleotide microarray mranscriptome analyses an interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae, J. Biol. Chem., 277, 37001, 10.1074/jbc.M204490200 Powell, 2007, Long term serial repitching and the genetic and phenotypic stability of brewer's yeast, J. Inst. Brew., 113, 67, 10.1002/j.2050-0416.2007.tb00258.x Powell, 2010, Serial repitching of dried lager yeast, J. Am. Soc. Brew. Chem., 68, 48 Powell, 2003, The impact of brewing yeast cell age on fermentation performance, attenuation and flocculation, FEMS Yeast Res., 3, 149, 10.1016/S1567-1356(03)00002-3 R Development Core Team, 2010 Rintala, 2011, Transcriptional responses of Saccharomyces cerevisiae to shift from respiratory and respirofermentative to fully fermentative metabolism, OMICS, 15, 461, 10.1089/omi.2010.0082 Rintala, 2009, Low oxygen levels as a trigger for enhancement of respiratory metabolism in Saccharomyces cerevisiae, BMC Genomics, 10, 461, 10.1186/1471-2164-10-461 Rintala, 2008, Transcription of hexose transporters of Saccharomyces cerevisiae is affected by change in oxygen provision, BMC Microbiol., 8, 53, 10.1186/1471-2180-8-53 Roberts, 2003, Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae, Mol. Biol. Cell, 14, 129, 10.1091/mbc.E02-08-0483 Roemer, 1994, Characterization of the yeast (1–>6)-beta-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly, J. Cell Biol., 127, 567, 10.1083/jcb.127.2.567 Ronnow, 1993, GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae, Yeast, 9, 1121, 10.1002/yea.320091013 Rossignol, 2009, The proteome of a wine yeast strain during fermentation, correlation with the transcriptome, J Appl. Microbiol., 107, 47, 10.1111/j.1365-2672.2009.04156.x Russell, 1983, Nucleotide sequence of the yeast alcohol dehydrogenase II gene, J. Biol. Chem., 258, 2674, 10.1016/S0021-9258(18)32979-X Saerens, 2007, Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation, Appl. Environ. Microbiol., 74, 454, 10.1128/AEM.01616-07 Saerens, 2008, Monitoring the influence of high-gravity brewing and fermentation temperature on flavour formation by analysis of gene expression levels in brewing yeast, Appl. Microbiol. Biotechnol., 80, 1039, 10.1007/s00253-008-1645-5 Sato, 2001, Genetic instability in flocculation of bottom-fermenting yeast, J. Am. Soc. Brew. Chem., 59, 130 Smart, 1995, Effect of serial repitching on the fermentation properties and condition of brewing yeast, J. Am. Soc. Brew. Chem., 54, 41 Strässer, 2001, Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p, Nature, 413, 648, 10.1038/35098113 Sturtz, 2001, A fraction of yeast Cu, Zn-superoxide dismutase and its metallochaperone CCS, localize to the intermembrane space of mitochondria: a physiological role for SOD1 in guarding against mitochondrial oxidative damage, J. Biol. Chem., 276, 38084, 10.1074/jbc.M105296200 Surana, 1991, The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae, Cell, 65, 145, 10.1016/0092-8674(91)90416-V Suzuki, 2002, Studies of cargo delivery to the vacuole mediated by autophagosomes in Saccharomyces cerevisiae, Dev. Cell, 3, 815, 10.1016/S1534-5807(02)00359-3 Ter Linde, 1999, Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae, J. Bacteriol., 181, 7409, 10.1128/JB.181.24.7409-7413.1999 Teste, 2009, Validation of reference genes for quantitative expression analysis by real-time RT-PCR in Saccharomyces cerevisiae, BMC Mol. Biol., 10, 99, 10.1186/1471-2199-10-99 Texeira, 1991, The influence of cell wall composition of a brewer's flocculent lager yeast on sedimentation during successive industrial fermentation, 241 Toda, 1988, SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits, Gene Dev., 2, 517, 10.1101/gad.2.5.517 Tsai, 2008, Afi1p functions as an Arf3p polarization-specific docking factor for development of polarity, J. Biol. Chem., 283, 16915, 10.1074/jbc.M802550200 van Loon, 1986, A yeast mutant lacking mitochondrial manganese-superoxide dismutase is hypersensitive to oxygen, PNAS, 83, 3820, 10.1073/pnas.83.11.3820 Van Mulders, 2009, Phenotypic diversity of Flo protein family-mediated adhesion in Saccharomyces cerevisiae, FEMS Yeast Res., 9, 178, 10.1111/j.1567-1364.2008.00462.x Van Wuytswinkel, 2000, Response of Saccharomyces cerevisiae to severe osmotic stress: evidence for a novel activation mechanism of the HOG MAP kinase pathway, Mol. Microbiol., 37, 382, 10.1046/j.1365-2958.2000.02002.x Vandesompele, 2002, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol., 3 Velours, 2002, Dual cell wall/mitochondria localization of the SUN family proteins, FEMS Microbiol. Lett., 207, 165, 10.1111/j.1574-6968.2002.tb11046.x Verbelen, 2009, Stability of high cell density brewery fermentations during serial repitching, Biotechnol. Lett., 31, 1729, 10.1007/s10529-009-0067-5 Verstrepen, 2003, Flavor-active esters: adding fruitiness to beer, J. Biosci. Bioeng., 96, 110, 10.1016/S1389-1723(03)90112-5 Warnes, 2011, 2, 10, 1 Westfall, 2004, When the stress of your environment makes you go HOG wild, Science, 306, 1511, 10.1126/science.1104879 Wiebe, 2008, Central carbon metabolism of Saccharomyces cerevisiae in anaerobic, oxygen-limited and fully aerobic steady-state conditions and following a shift to anaerobic conditions, FEMS Yeast Res., 8, 140, 10.1111/j.1567-1364.2007.00234.x Wills, 1976, Production of yeast alcohol dehydrogenase isoenzymes by selection, Nature, 261, 26, 10.1038/261026a0 Wilson, 2004, The 1.8-Å resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/PfpI superfamily, PNAS, 101, 1531, 10.1073/pnas.0308089100 Winderickx, 1996, Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control?, Molec. Gen. Genet., 252, 470 Yorimitsu, 2005, Autophagy: molecular machinery for self-eating, Cell Death Differ., 12, 1542, 10.1038/sj.cdd.4401765 Zhao, 2012, Zinc and yeast stress tolerance: micronutrient plays a big role, J. Biotech., 158, 176, 10.1016/j.jbiotec.2011.06.038