Synthetic genome engineering forging new frontiers for wine yeast

References

• Willetts D. Eight great technologies. London: Policy Exchange; 2013.
   Google Scholar
• Kelley NJ, Whelan DJ, Kerr E, et al. Engineering biology to address global problems: Synthetic Biology markets, needs, and applications. Industrial Biotechnol. 2014;10:140–149.
   Google Scholar
• Silva A, Yang H, Boeke JD, et al. Freedom and responsibility in synthetic genomics: The Synthetic Yeast Project. Genetics. 2015;200:1021–1028.
   PubMed Web of Science ®Google Scholar
• Lee D, Lloyd N, Pretorius IS, et al. Heterologous production of raspberry ketone in the wine yeast Saccharomyces cerevisiae via pathway engineering and synthetic enzyme fusion. Microb Cell Fact. 2016;15:49–55.
   PubMed Web of Science ®Google Scholar
• Cameron DE, Bashor CJ, Collins JJ. A brief history of synthetic biology. Nat Rev Microbiol. 2014;12:381–390.
   PubMed Web of Science ®Google Scholar
• Cello J, Paul AV, Wimmer E. Chemical synthesis of poliovirus cDNA: generation of infectious virus in the absence of natural template. Science. 2002;297:1016–1018.
   PubMed Web of Science ®Google Scholar
• Smith HO, Hutchison CA, Pfannkoch C, et al. Generating a synthetic genome by whole genome assembly: Phi-X174 bacteriophage from synthetic oligonucleotides. Proc Natl Acad Sci USA. 2003;100:15440–15445.
   PubMed Web of Science ®Google Scholar
• Gibson DG, Benders GA, Andrews-Pfannkoch C, et al. Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science. 2008;319:1215–1220.
   PubMed Web of Science ®Google Scholar
• Gibson DG, Glass JI, Lartigue C, et al. Creation of a bacterial cell controlled by a chemically synthesized genome. Science. 2010;329:52–56.
   PubMed Web of Science ®Google Scholar
• Gibson DG, Venter JG. Synthetic biology: construction of a yeast chromosome. Nature. 2014;509:168–169.
   PubMed Web of Science ®Google Scholar
• Hutchison CA, Chuang RY, Noskov VN, et al. Design and synthesis of a minimal bacterial genome. Science. 2016;351:6253–6255.
   Web of Science ®Google Scholar
• Isaacs FJ, Carr PA, Wang HH, et al. Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science. 2011;333:348–353.
   PubMed Web of Science ®Google Scholar
• Lajoie MJ, Rovner AJ, Goodman DB, et al. Genomically recoded organisms expand biological functions. Science. 2013;342:357–360.
   PubMed Web of Science ®Google Scholar
• Pennisi E. Building the ultimate yeast genome. Science. 2014;343:1426–1429.
   PubMed Web of Science ®Google Scholar
• Jolly NP, Varela C, Pretorius IS. Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res. 2014;14:215–237.
   PubMed Web of Science ®Google Scholar
• Pretorius IS D, Toit MD, Van Rensburg P. Designer yeasts for the fermentation industry of the 21st Century. Food Technol Biotechnol. 2003;41:3–10.
   Web of Science ®Google Scholar
• Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988;52:536–553.
   PubMedGoogle Scholar
• Jermy A. Milestones in synthetic (micro)biology. Nat Microbiol. 2014;12:309.
   Web of Science ®Google Scholar
• Chambers PJ, Pretorius IS. Fermenting knowledge: the history of winemaking, science and yeast research. EMBO Rep. 2010;11:1–7.
   PubMed Web of Science ®Google Scholar
• Pretorius IS, Curtin CD, Chambers PJ. The winemaker’s bug: from ancient wisdom to opening new vistas with frontier yeast science. Bioeng Bugs. 2012;3:147–156.
   PubMedGoogle Scholar
• Goffeau A, Barrell BG, Bussey H. Life with 6000 genes. Science. 1996;274:546–567.
   PubMed Web of Science ®Google Scholar
• Oliver SG. From DNA sequence to biological function. Nature. 1996;379:597–600.
   PubMed Web of Science ®Google Scholar
• Winzeler EA, Shoemaker DD, Astromoff A. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 1999;285:901–906.
   PubMed Web of Science ®Google Scholar
• Annaluru N, Muller H, Mitchell LA, et al. Total synthesis of a functional designer eukaryotic chromosome. Science. 2014;344:55–58.
   PubMed Web of Science ®Google Scholar
• Dymond JS, Richardson SM, Coombes CE, et al. Synthetic chromosome arms function in yeast and generate phenotypic diversity by design. Nature. 2011;477:471–476.
   PubMed Web of Science ®Google Scholar
• Hinnen A, Hicks JB, Fink GR. Transformation of yeast. Proc Natl Acad Sci USA. 1978;75:1929–1933.
   PubMed Web of Science ®Google Scholar
• Pretorius IS, Høj PB. Grape and wine biotechnology: challenges, opportunities and potential benefits. Austral J Grape Wine Res. 2005;11:83–108.
   Web of Science ®Google Scholar
• Borneman AR, Pretorius IS, Chambers PJ. Comparative genomics: a revolutionary tool for wine yeast strain development. Curr Opin Biotechnol. 2013;24:192–199.
   PubMed Web of Science ®Google Scholar
• Borneman AR, Schmidt SA, Pretorius IS. At the cutting-edge of grape and wine biotechnology. Trends Genet. 2013;29:263–271.
   PubMed Web of Science ®Google Scholar
• Williams CT, Pretorius IS, Paulsen PT. Synthetic evolution of metabolic productivity using biosensors. Trends Biotechnol. 2016;34:371–381.
   PubMed Web of Science ®Google Scholar
• David F, Siewers V. Advances in yeast genome engineering. FEMS Yeast Res. 2015;15:1–14. doi:10.1111/1567-1364.12200.
   PubMed Web of Science ®Google Scholar
• Kim IL, Roldão A, Siewers V, et al. A systems-level approach for metabolic engineering of yeast cell factories. FEMS Yeast Res. 2012;12:228–248.
   PubMed Web of Science ®Google Scholar
• Hansen EH, Møller BL, Kock GR, et al. De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and baker’s yeast (Saccharomyces cerevisiae). Appl Environ Microbiol. 2009;75:2765–2774.
   PubMed Web of Science ®Google Scholar
• Brochado AR, Matos C, Møller BL, et al. Improved vanillin production in baker’s yeast through in silico design. Microbial Cell Fact. 2010;9:1–15.
   PubMed Web of Science ®Google Scholar
• Brochado AR, Patil KR. Overexpression of O-methyltransferase leads to improved vanillin production in baker’s yeast only when complemented with model-guided network engineering. Biotechnol Bioeng. 2013;110:656–659.
   PubMed Web of Science ®Google Scholar
• Cankar K, Van Houwelingen A, Bosch D, et al. A chicory cytochrome P450 mono-oxygenase CYP71AV8 for the oxidation of (+)-valencene. FEBS Lett. 2011;585:178–182.
   PubMed Web of Science ®Google Scholar
• Gallage NJ, Møller BL. Vanillin bioconversion and bioengineering of the most popular plant flavour and its de novo biosynthesis in the vanilla orchid. Mol Plant. 2015;8:40–57.
   PubMed Web of Science ®Google Scholar
• Strucko T, Magnesko O, Mortensen UH. Benchmarking two commonly used Saccharomyces cerevisiae strains for heterologous vanillin-β-glucoside production. Metabolic Eng Comm. 2015;2:99–108.
   Google Scholar
• Becker VW, Armstrong GO, Van der Merwe MJ, et al. Metabolic engineering of Saccharomyces cerevisiae for the synthesis of the wine-related antioxidant resveratrol. FEMS Yeast Res. 2003;4:79–85.
   PubMed Web of Science ®Google Scholar
• Li M, Kildegaard KR, Chen Y, et al. De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae. Metab Eng. 2015;32:1–11.
   PubMed Web of Science ®Google Scholar
• Paddon CJ, Westfall PJ, Pitera DJ, et al. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature. 2013;496:528–532.
   PubMed Web of Science ®Google Scholar
• Andersen-Ranberg J, Kongstad KT, Nielsen MT, et al. Expanding the landscape of diterpene structural diversity through stereochemically controlled combinatorial biosynthesis. Angewandte Chem. 2016;128:2182–2186.
   Google Scholar
• Pretorius IS. Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast. 2000;16:675–729.
   PubMed Web of Science ®Google Scholar
• Verstrepen KJ, Chambers PJ, Pretorius IS. The development of superior yeast strains for the food and beverage industries: challenges, opportunities and potential benefits. In: Querol A, Fleet GH, editors. The yeast handbook: yeasts in food and beverages. Heidelberg: Springer; 2006. p. 399–444.
   Google Scholar
• Chambers PJ, Bellon JR, Schmidt SA, et al. (2009). Non-genetic engineering approaches to isolating and generating novel yeasts for industrial applications. In: Kunze G, Satyanarayana T, editors. Yeast biotechnology: diversity and applications. Berlin: Springer; 2009. p. 433–457.
   Google Scholar
• Cambon B, Monteil V, Remize F, et al. Effects of GPD1 overexpression in Saccharomyces cerevisiae commercial wine yeast strains lacking ALD6 genes. Appl Environ Microbiol. 2006;72:4688–4694.
   PubMed Web of Science ®Google Scholar
• De Barros Lopes MA, Rehman AU, Gockowiak H, et al. Fermentation properties of a wine yeast over-expressing the Saccharomyces cerevisiae glycerol 3-phosphate dehydrogenase gene (GPD2). Austral J Grape Wine Res. 2000;6:208–215.
   Google Scholar
• Eglinton JM, Heinrich AJ, Pollnitz AP, et al. Decreasing acetic acid accumulation by a glycerol overproducing strain of Saccharomyces cerevisiae by deleting the ALD6 aldehyde dehydrogenase gene. Yeast. 2002;19:295–301.
   PubMed Web of Science ®Google Scholar
• Kutyna DR, Varela C, Henschke PA, et al. Microbiological approaches to lowering ethanol concentration in wine. Trends Food Sci Technol. 2010;21:293–302.
   Web of Science ®Google Scholar
• Kutyna DR, Varela C, Stanley GA, et al. Adaptive evolution of Saccharomyces cerevisiae to generate strains with enhanced glycerol production. Appl Microbiol Biotechnol. 2012;93:1175–1184.
   PubMed Web of Science ®Google Scholar
• Michnick S, Roustan J-L, Remize F, et al. Modulation of glycerol and ethanol yields during alcoholic fermentation in Saccharomyces cerevisiae strains overexpressed or disrupted for GPD1 encoding glycerol 3-phosphate dehydrogenase. Yeast. 1997;13:783–793.
   PubMed Web of Science ®Google Scholar
• Remize F, Roustan J, Sablayrolles J, et al. Glycerol overproduction by engineered Saccharomyces cerevisiae wine yeast strains leads to substantial changes in by-product formation and to a stimulation of fermentation rate in stationary phase. Appl Environ Microbiol. 1999;65:143–149.
   PubMed Web of Science ®Google Scholar
• Tilloy V, Ortiz-Julien A, Dequin S. Reduction of ethanol yield and improvement of glycerol formation by adaptive evolution of the wine yeast Saccharomyces cerevisiae under hyperosmotic conditions. Appl Environ Microbiol. 2014;80:2623–2632.
   PubMed Web of Science ®Google Scholar
• Tilloy V, Cadiere A, Ehsani M, et al. Reducing alcohol levels in wines through rational and evolutionary engineering of Saccharomyces cerevisiae. Int J Food Microbiol. 2015;213:49–58.
   PubMed Web of Science ®Google Scholar
• Varela C, Kutyna DR, Solomon M, et al. Evaluation of gene modification strategies to develop low-alcohol wine yeasts. Appl Environ Microbiol. 2012;17:6068–6077.
   Web of Science ®Google Scholar
• Cordente AG, Heinrich AJ, Pretorius IS, et al. Isolation of sulfite reductase variants of a commercial wine yeast with significantly reduced hydrogen sulfide production. FEMS Yeast Res. 2009;9:446–459.
   PubMed Web of Science ®Google Scholar
• Cordente AG, Curtin CD, Varela C, et al. Flavour-active wine yeasts. Appl Microbiol Biotechnol. 2012;96:601–618.
   PubMed Web of Science ®Google Scholar
• Luo Z, Walkey CJ, Madilao LL, et al. Functional improvement of Saccharomyces cerevisiae to reduce volatile acidity in wine. FEMS Yeast Res. 2013;13:485–494.
   PubMed Web of Science ®Google Scholar
• Lilly M, Bauer FF, Lambrechts MG, et al. The effect of increased yeast alcohol acetyltransferase and esterase activity on the flavour profiles of wine and distillates. Yeast. 2006;23:641–659.
   PubMed Web of Science ®Google Scholar
• Lilly M, Styger G, Bauer FF, et al. The effect of increased yeast branched-chain amino acid transaminase activity and the production of higher alcohols on the flavor profiles of wine and distillates. FEMS Yeast Res. 2006;6:726–743.
   PubMed Web of Science ®Google Scholar
• Carrau FM, Medina K, Boido E, et al. De novo synthesis of monoterpenes by Saccharomyces cerevisiae wine yeasts. FEMS Microbiol Lett. 2005;243:107–115.
   PubMed Web of Science ®Google Scholar
• Cordente AG, Cordero-Bueso G, Pretorius IS, et al. Novel wine yeast with mutations in YAP1 that produce less acetic acid during fermentation. FEMS Yeast Res. 2013;13:62–73.
   PubMed Web of Science ®Google Scholar
• Holt S, Cordente AG, Williams SJ, et al. Engineering Saccharomyces cerevisiae to release 3-mercaptohexan-1-ol during fermentation through overexpression of an S. cerevisiae gene, STR3, for improvement of wine aroma. Appl Environ Microbiol. 2011;77:3626–3632.
   PubMed Web of Science ®Google Scholar
• Roncoroni M, Santiago M, Hooks DO, et al. The yeast IRC7 gene encodes a β-lyase responsible for production of the varietal thiol 4-mercapto-4-methylpentan-2-one in wine. Food Microbiol. 2011;28:926–935.
   PubMed Web of Science ®Google Scholar
• Swiegers JH, Bartowsky EJ, Henschke PA, et al. Yeast and bacterial modulation of wine aroma and flavour. Austral J Grape Wine Res. 2005;11:139–173.
   Web of Science ®Google Scholar
• Swiegers JH, Capone DL, Pardon KH, et al. Engineering volatile thiol release in Saccharomyces cerevisiae for improved wine aroma. Yeast. 2007;24:561–574.
   PubMed Web of Science ®Google Scholar
• Swiegers JH, Pretorius IS. Modulation of volatile sulfur compounds by wine yeast. Appl Microbiol Biotechnol. 2007;74:954–960.
   PubMed Web of Science ®Google Scholar
• Swiegers JH, Saerens SMG, Pretorius IS. Novel yeast strains as tools to adjust the flavour of fermented beverages to market specifications. In: Frenkel DH, Belanger F, editors. Biotechnology in flavour production. Oxford: Blackwell Publishing; 2008. p. 1–55.
   Google Scholar
• Swiegers JH, Kievit RL, Siebert T, et al. The influence of yeast on the aroma of Sauvignon Blanc wine. Food Microbiol. 2009;26:204–211.
   PubMed Web of Science ®Google Scholar
• Thibon C, Marullo P, Claisse O, et al. Nitrogen catabolic repression controls the release of volatile thiols by Saccharomyces cerevisiae during wine fermentation. FEMS Yeast Res. 2008;8:1076–1086.
   PubMed Web of Science ®Google Scholar
• Wood C, Siebert TE, Parker M, et al. From wine to pepper: rotundone, an obscure sesquiterpene, is a potent spicy aroma compound. J Agric Food Chem. 2008;56:3738–3744.
   PubMed Web of Science ®Google Scholar
• Takahashi S, Yeo Y, Greenhagen BT, et al. Metabolic engineering of sesquiterpene metabolism in yeast. Biotechnol Bioeng. 2007;97:170–181.
   PubMed Web of Science ®Google Scholar
• Takase H, Sasaki K, Shinmori H, et al. Cytochrome P450 CYP71BE5 in grapevine (Vitis vinifera) catalyzes the formation of the spicy aroma compound (−)-rotundone. J Exp Bot. 2016;67:787–798.
   PubMed Web of Science ®Google Scholar
• Volschenk H, Viljoen-Bloom M, Van Staden J, et al. Genetic engineering of an industrial strain of Saccharomyces cerevisiae for l-malic acid degradation via an efficient malo-ethanolic pathway. S Afr J Enol Vitic. 2004;25:63–73.
   Google Scholar
• Husnik JI, Volschenk H, Bauer F, et al. Metabolic engineering of malolactic wine yeast. Metabolic Eng. 2006;8:315–323.
   PubMed Web of Science ®Google Scholar
• Coulon J, Husnik JI, Inglis DL, et al. Metabolic engineering of Saccharomyces cerevisiae to minimize the production of ethyl carbamate in wine. Am J Enol Vitic. 2006;57:113–124.
   Web of Science ®Google Scholar
• Pretorius IS, Bauer FF. Meeting the consumer challenge through genetically customized wine-yeast strains. Trends Biotechnol. 2002;20:426–432.
   PubMed Web of Science ®Google Scholar
• Pretorius IS, Curtin CD, Chambers PJ. Designing wine yeast for the future. In: Holzapfel W, editor. Advances in fermented foods and beverages: improving quality, technologies and health benefits. Cambridge: Woodhead Publishing; 2015. p. 195–226.
   Google Scholar
• Borneman AR, Forgan AH, Pretorius IS, et al. Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res. 2008;8:1185–1195.
   PubMed Web of Science ®Google Scholar
• Borneman AR, Desany BA, Riches D, et al. Whole genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet. 2011;7:e1001287.
   PubMed Web of Science ®Google Scholar
• Borneman AR, Desany BA, Riches D, et al. The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res. 2012;12:88–96.
   PubMed Web of Science ®Google Scholar
• Dunn B, Richter C, Kvitek DJ, et al. Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res. 2012;22:908–924.
   PubMed Web of Science ®Google Scholar
• Galeote V, Novo M, Salema-Oom M, et al. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H + symporter. Microbiology. 2010;56:3754–3761.
   Web of Science ®Google Scholar
• Galeote V, Bigey F, Beyne E, et al. Amplification of a Zygosaccharomyces bailii DNA segment in wine yeast genomes by extrachromosomal circular DNA formation. PLoS One. 2011;6:e17872.
   PubMed Web of Science ®Google Scholar
• Novo M, Bigey F, Beyne E, et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci USA. 2009;106:16333–16338.
   PubMed Web of Science ®Google Scholar
• Wei W, McCusker JH, Hyman RW, et al. Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc Natl Acad Sci USA. 2007;104:12825–12830.
   PubMed Web of Science ®Google Scholar
• Liti G, Carter DM, Moses AM, et al. Population genomics of domestic and wild yeasts. Nature. 2009;458:337–341.
   PubMed Web of Science ®Google Scholar
• Borneman AR, Pretorius IS. Genomic insights into the Saccharomyces sensu stricto complex. Genetics. 2015;199:281–291.
   PubMed Web of Science ®Google Scholar
• Zabetakis I, Holden MA. Strawberry flavour: analysis and biosynthesis. J Sci Food Agric. 1997;74:421–434.
   Web of Science ®Google Scholar
• Beekwilder J, van der Meer IM, Sibbesen O. Microbial production of natural raspberry ketone. Biotechnol J. 2007;2:1270–1279.
   PubMedGoogle Scholar
• Nielsen J, Keasling JD. Synergies between synthetic biology and metabolic engineering. Nat Biotechnol. 2011;29:693–695.
   PubMed Web of Science ®Google Scholar