Abstract
Producers often utilise some of the many available yeast species and strains in the making of fermented alcoholic beverages in order to augment flavours, aromas, acids and textural properties. But still, the demand remains for more yeasts with novel phenotypes that not only impact sensory characteristics but also offer process and engineering advantages. Two strategies for finding such yeasts are (i) bioprospecting for novel strains and species and (ii) genetic modification of known yeasts. The latter enjoys the promise of the emerging field of synthetic biology, which, in principle, would enable scientists to create yeasts with the exact phenotype desired for a given fermentation. In this mini review, we compare and contrast advances in bioprospecting and in synthetic biology as they relate to alcoholic fermentation in brewing and wine making. We explore recent advances in fermentation-relevant recombinant technologies and synthetic biology including the Yeast 2.0 Consortium, use of environmental yeasts, challenges, constraints of law and consumer acceptance.
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References
Albergaria H, Arneborg N (2016) Dominance of Saccharomyces cerevisiae in alcoholic fermentation processes: role of physiological fitness and microbial interactions. Appl Microbiol Biotech 100(5):2035–2046. https://doi.org/10.1007/s00253-015-7255-0
Andrich L, Esti M, Moresi M (2009) Urea degradation in model wine solutions by free or immobilized acid urease in a stirred bioreactor. J Ag Food Chem 57(9):3533–3342. https://doi.org/10.1021/jf803962b
Anfang N, Brajkovich M, Goddard MR (2009) Co-fermentation with Pichia kluyveri increases varietal thiol concentrations in Sauvignon Blanc. Aust J Grape Wine Res 15(1):1–8. https://doi.org/10.1111/j.1755-0238.2008.00031.x
Ansanay V, Dequin S, Camarasa C, Schaeffer V, Grivet J, Blondin B, Salmon J, Barre P (1996) Malolactic fermentation by engineered Saccharomyces cerevisiae as compared with engineered Schizosaccharomyces pombe. Yeast 12:215–225. https://doi.org/10.1002/(SICI)1097-0061(19960315)12:3<215::AID-YEA903>3.0.CO;2-M
Aponte M, Blaiotta G (2016) Potential role of yeast strains isolated from grapes in the production of Taurasi DOCG. Front Microbiol 7:809. https://doi.org/10.3389/fmicb.2016.00809
Azzolini M, Tosi E, Lorenzini M, Finato F, Zapparoli G (2015) Contribution to the aroma of white wines by controlled Torulaspora delbrueckii cultures in association with Saccharomyces cerevisiae. W J Microbiol Biotech 31(2):277–293. https://doi.org/10.1007/s11274-014-1774-1
Baeshen NA, Baeshen MN, Sheikh A, Bora RS, Ahmed MMM, Ramadan HAI, Saini KS, Redwan EM (2014) Cell factories for insulin production. Microb Cell Factories 13:141–141. https://doi.org/10.1186/s12934-014-0141-0
Baffi MA, Tobal T, Lago JHG, Boscolo M, Gomes E, Da-Silva R (2013) Wine aroma improvement using a β-glucosidase preparation from Aureobasidium pullulans. Appl Biochem Biotech 169(2):493–501. https://doi.org/10.1007/s12010-012-9991-2
Barnett JA (2004) A history of research on yeasts 8: taxonomy. Yeast 21(14):1141–1193. https://doi.org/10.1002/yea.1154
Basso RF, Alcarde AR, Portugal CB (2016) Could non-Saccharomyces yeasts contribute on innovative brewing fermentations? Food Res Int 86:112–120. https://doi.org/10.1016/j.foodres.2016.06.002
Bayly FC, Berg HW (1967) Grape and wine proteins of white wine varietals. Am J Enol Vitic 18(1):18–32
Belda I, Ruiz J, Alastruey-Izquierdo A, Navascues E, Marquina D, Santos A (2016) Unraveling the enzymatic basis of wine “Flavorome”: a phylo-functional study of wine related yeast species. Front Microbiol 7:12. https://doi.org/10.3389/fmicb.2016.00012
Belloch C, Pérez-Torrado R, González SS, Pérez-Ortín JE, García-Martínez J, Querol A, Barrio E (2009) Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Appl Environl Microbiol 75(8):2534–2544. https://doi.org/10.1128/aem.02282-08
Benito Á, Jeffares D, Palomero F, Calderón F, Bai F-Y, Bähler J, Benito S (2016) Selected Schizosaccharomyces pombe strains have characteristics that are beneficial for winemaking. PLoS One 11(3):e0151102–e0151102. https://doi.org/10.1371/journal.pone.0151102
Berman AY, Motechin RA, Wiesenfeld MY, Holz MK (2017) The therapeutic potential of resveratrol: a review of clinical trials. npj Precis Oncol 1(1):35. https://doi.org/10.1038/s41698-017-0038-6
Berner TS, Jacobsen S, Arneborg N (2013) The impact of different ale brewer’s yeast strains on the proteome of immature beer. BMC Microbiol 13:215–215. https://doi.org/10.1186/1471-2180-13-215
Bokulich NA, Bamforth CW (2013) The microbiology of malting and brewing. Microbiol Mol Biol Rev 77(2):157–172. https://doi.org/10.1128/MMBR.00060-12
Bokulich NA, Thorngate JH, Richardson PM, Mills DA (2014) Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. PNAS 111(1):E139–E148. https://doi.org/10.1073/pnas.1317377110
Boss PK, Pearce AD, Zhao Y, Nicholson EL, Dennis EG, Jeffery DW (2015) Potential grape-derived contributions to volatile ester concentrations in wine. Molecules 20(5):7845–7873. https://doi.org/10.3390/molecules20057845
Brady M (2008) First taste. How indigenous Australians learned about grog. AER Foundation, Canberra
Bruwer J, Chrysochou P, Lesschaeve I (2017) Consumer involvement and knowledge influence on wine choice cue utilisation. Brit Food J 119:830–844. https://doi.org/10.1108/BFJ-08-2016-0360
Buzzini P, Martini A (2002) Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments. J Appl Microbiol 93(6):1020–1025
Cai P, Gao J, Zhou Y (2019) CRISPR-mediated genome editing in non-conventional yeasts for biotechnological applications. Microb Cell Factories 18:63. https://doi.org/10.1186/s12934-019-1112-2
Capozzi V, Garofalo C, Chiriatti MA, Grieco F, Spano G (2015) Microbial terroir and food innovation: the case of yeast biodiversity in wine. Microbiol Res 181:75–83. https://doi.org/10.1016/j.micres.2015.10.005
Carrasco M, Rozas JM, Barahona S, Alcaíno J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12(1):251. https://doi.org/10.1186/1471-2180-12-251
Chambers PJ, Pretorius IS (2010) Fermenting knowledge: the history of winemaking, science and yeast research. EMBO Rep 11(12):914–920. https://doi.org/10.1038/embor.2010.179
Chen SJ (2019) Minimizing off-target effects in CRISPR-Cas9 genome editing. Cell Biol Toxicol 35:399–401. https://doi.org/10.1007/s10565-019-09486-4
Ciani M, Comitini F (2011) Non-Saccharomyces wine yeasts have a promising role in biotechnological approaches to winemaking. Annals Microbiol 61(1):25–32. https://doi.org/10.1007/s13213-010-0069-5
Ciani M, Capece A, Comitini F, Canonico L, Siesto G, Romano P (2016) Yeast interactions in inoculated wine fermentation. Front Microbiol 7(555). https://doi.org/10.3389/fmicb.2016.00555
Claus H, Mojsov K (2018) Enzymes for wine fermentation: current and perspective applications. Ferment 4(3):52
Clemente-Jimenez JM, Mingorance-Cazorla L, Martı́nez-Rodrı́guez S, Las Heras-Vázquez FJ, Rodrı́guez-Vico F (2004) Molecular characterization and oenological properties of wine yeasts isolated during spontaneous fermentation of six varieties of grape must. Food Microbiol 21(2):149-155. https://doi.org/10.1016/S0740-0020(03)00063-7
Combina M, Elía A, Mercado L, Catania C, Ganga A, Martinez C (2005) Dynamics of indigenous yeast populations during spontaneous fermentation of wines from Mendoza, Argentina. Int J Food Microbiol 99(3):237–243. https://doi.org/10.1016/j.ijfoodmicro.2004.08.017
Contreras A, Hidalgo C, Henschke PA, Chambers PJ, Curtin C, Varela C (2014) Evaluation of non-Saccharomyces yeasts for the reduction of alcohol content in wine. Appl Environ Microbiol 80(5):1670–1678. https://doi.org/10.1128/AEM.03780-13
Coulon J, Husnik JI, Inglis DL, van der Merwe GK, Lonvaud A, Erasmus DJ, van Vuuren HJJ (2006) Metabolic engineering of Saccharomyces cerevisiae to minimize the production of ethyl carbamate in wine. Am J Enol Vitic 57(2):113–124
Cray JA, Bell ANW, Bhaganna P, Mswaka AY, Timson DJ, Hallsworth JE (2013) The biology of habitat dominance; can microbes behave as weeds? Microb Biotechnol 6(5):453–492. https://doi.org/10.1111/1751-7915.12027
Curiel JA, Morales P, Gonzalez R, Tronchoni J (2017) Different non-Saccharomyces yeast species stimulate nutrient consumption in S. cerevisiae mixed cultures. Front Microbiol 8:2121–2121. https://doi.org/10.3389/fmicb.2017.02121
De Francesco G, Turchetti B, Sileoni V, Marconi O, Perretti G (2015) Screening of new strains of Saccharomycodes ludwigii and Zygosaccharomyces rouxii to produce low-alcohol beer. J Inst Brew 121(1):113–121. https://doi.org/10.1002/jib.185
De Francesco G, Sannino C, Sileoni V, Marconi O, Filippucci S, Tasselli G, Turchetti B (2018) Mrakia gelida in brewing process: an innovative production of low alcohol beer using a psychrophilic yeast strain. Food Microbiol 76:354–362. https://doi.org/10.1016/j.fm.2018.06.018
de Ponzzes-Gomes CM, de Mélo DLFM, Santana CA, Pereira GE, Mendonça MOC, Gomes FCO, Oliveira ES, Barbosa AM, Trindade RC, Rosa CA (2014) Saccharomyces cerevisiae and non-Saccharomyces yeasts in grape varieties of the São Francisco Valley. Braz J Microbiol 45(2):411–416
Denby CM, Li RA, Vu VT, Costello Z, Lin W, Chan LJG, Williams J, Donaldson B, Bamforth CW, Petzold CJ, Scheller HV, Martin HG, Keasling JD (2018) Industrial brewing yeast engineered for the production of primary flavor determinants in hopped beer. Nat Commun 9(1):965. https://doi.org/10.1038/s41467-018-03293-x
Diderich JA, Weening SM, van den Broek M, Pronk JT, Daran JMG (2018) Selection of Pof-Saccharomyces eubayanus variants for the construction of S. cerevisiae × S. eubayanus hybrids with reduced 4-vinyl guaiacol formation. Front Microbiol 9:1640. https://doi.org/10.3389/fmicb.2018.01640
Ding S, Zhang Y, Zhang J, Zeng W, Yang Y, Guan J, Pan L, Li W (2015) Enhanced deacidification activity in Schizosaccharomyces pombe by genome shuffling. Yeast 32:317–325. https://doi.org/10.1002/yea.3053
Domizio P, House JF, Joseph CML, Bisson LF, Bamforth CW (2016) Lachancea thermotolerans as an alternative yeast for the production of beer. J Inst Brew 122(4):599-604. https://doi.org/10.1002/jib.362
Dymond J, Boeke J (2012) The Saccharomyces cerevisiae SCRaMbLE system and genome minimization. Bioeng Bugs 3(3):168–171. https://doi.org/10.4161/bbug.19543
Eriksson D, Harwood W, Hofvander P, Jones H, Rogowsky P, Stöger E, Visser RGF (2018) A welcome proposal to amend the GMO legislation of the EU. Trends Biotech 36:1100–1103. https://doi.org/10.1016/j.tibtech.2018.05.001
Estela-Escalante WD, Moscosa-Santillán M, González-Ramírez JE, Rosales-Mendoza S (2017) Evaluation of the potential production of ethanol by Candida zemplinina yeast with regard to beer fermentation. J Am Soc Brew Chem 75(2):130–135. https://doi.org/10.1094/ASBCJ-2017-2532-01
Fleet GH (1990) Growth of yeasts during wine fermentations. J Wine Res 1(3):211–223. https://doi.org/10.1080/09571269008717877
Fleiss A, O'Donnell S, Fournier T, Lu W, Agier N, Delmas S, Schacherer J, Fischer G (2019) Reshuffling yeast chromosomes with CRISPR/Cas9. PLoS Genet 15(8):e1008332. https://doi.org/10.1371/journal.pgen.1008332
García M, Esteve-Zarzoso B, Crespo J, Cabellos JM, Arroyo T (2017) Yeast monitoring of wine mixed or sequential fermentations made by native strains from D.O. “Vinos de Madrid” using real-time quantitative PCR. Front Microbiol 8:2520. https://doi.org/10.3389/fmicb.2017.02520
García-Ríos E, Guillén A, de la Cerda R, Pérez-Través L, Querol A, Guillamón JM (2019) Improving the cryotolerance of wine yeast by interspecific hybridization in the genus Saccharomyces. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.03232
Gibson B, Geertman JMA, Hittinger CT, Krogerus K, Libkind D, Louis EJ, Magalhães F, Sampaio JP (2017) New yeasts—new brews: modern approaches to brewing yeast design and development. FEMS Yeast Res 17(4):38–42. https://doi.org/10.1093/femsyr/fox038
Gilliam M, Wickerham LJ, Morton HL, Martin RD (1974) Yeasts isolated from honey bees, Apis mellifera, fed 2,4-D and antibiotics. J Invert Pathol 24(3):349–356. https://doi.org/10.1016/0022-2011(74)90143-8
Gorter de Vries AR, Pronk JT, Daran JG (2019) Lager-brewing yeasts in the era of modern genetics. FEMS Yeast Res 19(7):foz063. https://doi.org/10.1093/femsyr/foz063
Gschaedler A (2017) Contribution of non-conventional yeasts in alcoholic beverages. Cur Op Food Sci 13:73–77. https://doi.org/10.1016/j.cofs.2017.02.004
Hammond JR (1995) Genetically-modified brewing yeasts for the 21st century. Progress to date Yeast 11:1613–1627. https://doi.org/10.1002/yea.320111606
Henschke PA, Jiranek V (1993) In: Fleet GH (ed) Yeasts - metabolism of nitrogen compounds. Wine microbiology and biotechnology, Chur, pp 77–164
Herrero Ó, Ramón D, Orejas M (2008) Engineering the Saccharomyces cerevisiae isoprenoid pathway for de novo production of aromatic monoterpenes in wine. Metabol Eng 10(2):78–86. https://doi.org/10.1016/j.ymben.2007.11.001
Hittinger CT, Steele JL, Ryder DS (2018) Diverse yeasts for diverse fermented beverages and foods. Cur Op Biotech 49:199–206. https://doi.org/10.1016/j.copbio.2017.10.004
Holt S, Mukherjee V, Lievens B, Verstrepen KJ, Thevelein JM (2018) Bioflavoring by non-conventional yeasts in sequential beer fermentations. Food Microbiol 72:55–66. https://doi.org/10.1016/j.fm.2017.11.008
Hranilovic A, Gambetta JM, Schmidtke L, Boss PK, Grbin PR, Masneuf-Pomarede I, Bely M, Albertin W, Jiranek V (2018) Oenological traits of Lachancea thermotolerans show signs of domestication and allopatric differentiation. Sci Rep 8(1):14812. https://doi.org/10.1038/s41598-018-33105-7
Hsu JC, Heatherbell DA (1987) Heat-unstable proteins in wine. Characterization and removal by bentonite fining and heat treatment. Am J Enol Vitic 38(1):11–16
Hsu D, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278. https://doi.org/10.1016/j.cell.2014.05.010
Husnik JI, Delaquis PJ, Cliff MA, van Vuuren HJJ (2007) Functional analyses of the malolactic wine yeast ML01. Am J Enol Vitic 58(1):42–52
Iolanda R, Vinella M, Domizio P (1994) Characterization of β-glucosidase activity in yeasts of oenological origin. J Appl Bacteriol 77(5):519–527. https://doi.org/10.1111/j.1365-2672.1994.tb04396.x
Ivey M, Massel M, Phister TG (2013) Microbial interactions in food fermentations. Annu Rev Food Sci Technol 4:141–162. https://doi.org/10.1146/annurev-food-022811-101219
Jagtap UB, Jadhav JP, Bapat VA, Pretorius IS (2017) Synthetic biology stretching the realms of possibility in wine yeast research. Int J Food Microbiol 252:24–34. https://doi.org/10.1016/j.ijfoodmicro.2017.04.006
Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res 14(2):215–237. https://doi.org/10.1111/1567-1364.12111
Kang YM, Choi JE, Komakech R, Park JH, Kim DW, Cho KM, Kang SM, Choi SH, Song KC, Ryu CM, Lee KC, Lee JS (2017) Characterization of a novel yeast species Metschnikowia persimmonesis KCTC 12991BP (KIOM G15050 type strain) isolated from a medicinal plant, Korean persimmon calyx. AMB Expr 7(1):199. https://doi.org/10.1186/s13568-017-0503-1
Kántor A, Hutková J, Petrová J, Hleba L, Kacaniova M (2015) Antimicrobial activity of pulcherrimin pigment produced by Metschnikowia pulcherrima against various yeast species. J Microbiol Biotech Food Sci 5:282–285. https://doi.org/10.15414/jmbfs.2015/16.5.3.282-285
Kitagaki H, Kitamoto K (2013) Breeding research on sake yeasts in Japan: history, recent technological advances, and future perspectives. Annual Rev Food Sci Tech 4:215–235. https://doi.org/10.1146/annurev-food-030212-182545
Klassen R, Schaffrath R, Buzzini P, Ganter PF (2017) Antagonistic interactions and killer yeasts. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: ecology. Springer, Cham
Krogerus K, Magalhaes F, Vidgren V, Gibson B (2015) New lager yeast strains generated by interspecific hybridization. J Ind Microbiol Biotechnol 42(5):769–778. https://doi.org/10.1007/s10295-015-1597-6
Krogerus K, Seppänen-Laakso T, Castillo S, Gibson B (2017) Inheritance of brewing-relevant phenotypes in constructed Saccharomyces cerevisiae × Saccharomyces eubayanus hybrids. Microb Cell Factories 16:66. https://doi.org/10.1186/s12934-017-0679-8
Krogerus K, Preiss R, Gibson B (2018) A unique Saccharomyces cerevisiae × Saccharomyces uvarum hybrid isolated from Norwegian farmhouse beer: characterization and reconstruction. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02253
Kutty SN, Philip R (2008) Marine yeasts — a review. Yeast 25(7):465–483. https://doi.org/10.1002/yea.1599
Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JS, Janzen DH (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1(1):1–8
Lallemand (2018) FLAVIA® MP346 product data sheet
Lallemand (2019) Sourvisiae product data sheet
Lambrechts M, Pretorius I (2000) Yeast and its importance to wine aroma - a review. Enol Vitic 21:139–173
Lee D, Lloyd NDR, Pretorius IS, Borneman AR (2016) Heterologous production of raspberry ketone in the wine yeast Saccharomyces cerevisiae via pathway engineering and synthetic enzyme fusion. Microb Cell Factories 15:49–49. https://doi.org/10.1186/s12934-016-0446-2
Libkind D, Diéguez MC, Moliné M, Pérez P, Zagarese HE, Broock M (2006) Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of northwestern Patagonia (Argentina). Photochem Photobiol 82(4):972–980. https://doi.org/10.1562/2005-09-09-RA-679
Lin MM-H, Boss PK, Walker ME, Sumby KM, Grbin PR, Jiranek V (2020) Evaluation of indigenous non-Saccharomyces yeasts isolated from a South Australian vineyard for their potential as wine starter cultures. Int J Food Microbiol 312:108373. https://doi.org/10.1016/j.ijfoodmicro.2019.108373
Liti G (2015) The fascinating and secret wild life of the budding yeast S. cerevisiae. eLife 4:e5835. https://doi.org/10.7554/eLife.05835
Lockshin L, Corsi AM (2012) Consumer behaviour for wine 2.0: a review since 2003 and future directions. Wine Econ Policy 1(1):2–23. https://doi.org/10.1016/j.wep.2012.11.003
Lodolo EJ, Kock JLF, Axcell BC, Brooks M (2008) The yeast Saccharomyces cerevisiae – the main character in beer brewing. FEMS Yeast Res 8(7):1018–1036. https://doi.org/10.1111/j.1567-1364.2008.00433.x
López-Malo M, García-Rios E, Melgar B, Sanchez MR, Dunham MJ, Guillamón JM (2015) Evolutionary engineering of a wine yeast strain revealed a key role of inositol and mannoprotein metabolism during low-temperature fermentation. BMC Genomics 16:537. https://doi.org/10.1186/s12864-015-1755-2
Luo Z, Wang L, Wang Y, Zhang W, Guo Y, Shen Y, Jiang L, Wu Q, Zhang C, Cai Y, Dai J (2018) Identifying and characterizing SCRaMbLEd synthetic yeast using ReSCuES. Nat Comms 9:1930. https://doi.org/10.1038/s41467-017-00806-y
Ma L, Li Y, Chen X, Ding M, Wu Y, Yuan YJ (2019) SCRaMbLE generates evolved yeasts with increased alkali tolerance. Microb Cell Factories 18:52–11. https://doi.org/10.1186/s12934-019-1102-4
Madden AA, Epps MJ, Fukami T, Irwin RE, Sheppard J, Sorger DM, Dunn RR (2018) The ecology of insect–yeast relationships and its relevance to human industry. Royal Soc Bio Sci 285(1875):2017–2733. https://doi.org/10.1098/rspb.2017.2733
Mallapaty S (2019) Australian gene-editing rules adopt ‘middle ground’: nature news. https://doi.org/10.1038/d41586-019-01282-8
Matthews A, Grimaldi A, Walker M, Bartowsky E, Grbin P, Jiranek V (2004) Lactic acid bacteria as a potential source of enzymes for use in vinification. Appl Environ Microbiol 70(10):5715–5731. https://doi.org/10.1128/AEM.70.10.5715-5731.2004
Maurizio C, Francesca C, Ilaria M, Paola D (2010) Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10(2):123-133. https://doi.org/10.1111/j.1567-1364.2009.00579.x
Meneses FJ, Henschke PA, Jiranek V (2002) A survey of industrial strains of Saccharomyces cerevisiae reveals numerous altered patterns of maltose and sucrose utilisation. J Inst Brew 108(3):310–321. https://doi.org/10.1002/j.2050-0416.2002.tb00556.x
Mojsov K (2013) Use of enzymes in wine making: a review. Int J Market Technol 3:112–127
Monerawela C, Bond U (2018) The hybrid genomes of Saccharomyces pastorianus: a current perspective. Yeast 35:39–50. https://doi.org/10.1002/yea.3250
Moreira N, Mendes F, Guedes de Pinho P, Hogg T, Vasconcelos I (2008) Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. Int J Food Microbiol 124(3):231–238. https://doi.org/10.1016/j.ijfoodmicro.2008.03.025
Mylona AE, Del Fresno JM, Palomero F, Loira I, Banuelos MA, Morata A, Calderon F, Benito S, Suarez-Lepe JA (2016) Use of Schizosaccharomyces strains for wine fermentation - effect on the wine composition and food safety. Int J Food Microbiol 232:63–72. https://doi.org/10.1016/j.ijfoodmicro.2016.05.023
Olaniran AO, Hiralal L, Mokoena MP, Pillay B (2017) Flavour-active volatile compounds in beer: production, regulation and control. J Inst Brew 123(1):13–23. https://doi.org/10.1002/jib.389
Oro L, Canonico L, Marinelli V, Ciani M, Comitini F (2019) Occurrence of Brettanomyces bruxellensis on grape berries and in related winemaking cellar. Front Microbiol:10. https://doi.org/10.3389/fmicb.2019.00415
Osburn K, Amaral J, Metcalf SR, Nickens DM, Rogers CM, Sausen C, Caputo R, Miller J, Li H, Tennessen J, Bochman M (2017) Primary souring: a novel bacteria-free method for sour beer production. J Food Microbiol 70:76–84. https://doi.org/10.1016/j.fm.2017.09.007
Pardo E, Rico J, Gil JV, Orejas M (2015) De novo production of six key grape aroma monoterpenes by a geraniol synthase-engineered S. cerevisiae wine strain. Microb Cell Factories 14:136–136. https://doi.org/10.1186/s12934-015-0306-5
Pflaum T, Hausler T, Baumung C, Ackermann S, Kuballa T, Rehm J, Lachenmeier DW (2016) Carcinogenic compounds in alcoholic beverages: an update. Arch Toxicol 90(10):2349–2367. https://doi.org/10.1007/s00204-016-1770-3
Pocock KF, HoJ PB, Adams KS, Kwiatkowski MJ, Waters E (2008) Combined heat and proteolytic enzyme treatment of white wines reduce haze forming protein content without detrimental effect. Aust J Grape Wine Res 9(1):56–63
Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16(8):675–729. https://doi.org/10.1002/1097-0061(20000615)
Pretorius IS, Boeke JD (2018) Yeast 2.0—connecting the dots in the construction of the world’s first functional synthetic eukaryotic genome. FEMS Yeast Res 18(4):foy032. https://doi.org/10.1093/femsyr/foy032
Rainieri S, Zambonelli C, Kaneko Y (2003) Saccharomyces sensu stricto: systematics, genetic diversity and evolution. J Biosci Bioeng 96(1):1–9
Rank GH, Casey G, Xiao W (1988) Gene transfer in industrial Saccharomyces yeasts. Food Biotechnol 2(1):1–41. https://doi.org/10.1080/08905438809549674
Rankine BC (1972) Influence of yeast strain and malo-lactic fermentation on composition and quality of table wines. Am J of Enol Vitic 23(4):152–158
Rantsiou K, Dolci P, Giacosa S, Torchio F, Tofalo R, Torriani S, Suzzi G, Rolle L, Cocolin L (2012) Candida zemplinina can reduce acetic acid produced by Saccharomyces cerevisiae in sweet wine fermentations. Appl Environ Microbiol 78(6):1987-1994. https://doi.org/10.1128/AEM.06768-11
Rao RS, Bhadra B, Shivaji S (2008) Isolation and characterization of ethanol-producing yeasts from fruits and tree barks. Lett Appl Microbiol 47(1):19–24. https://doi.org/10.1111/j.1472-765X.2008.02380.x
Rementeria A, Rodriguez JA, Cadaval A, Amenabar R, Muguruza JR, Hernando FL, Sevilla MJ (2003) Yeast associated with spontaneous fermentations of white wines from the “Txakoli de Bizkaia” region (Basque Country, North Spain). Int J Food Microbiol 86(1):201–207. https://doi.org/10.1016/S0168-1605(03)00289-7
Richardson SM, Mitchell LA, Stracquadanio G, Yang K, Dymond JS, DiCarlo JE, Lee D, Huang CL, Chandrasegaran S, Cai Y, Boeke JD, Bader JS (2017) Design of a synthetic yeast genome. Sci 355:1040–1044. https://doi.org/10.1126/science.aaf4557
Ristic R, Hranilovic A, Li S, Longo R, Pham D-T, Qesja B, Jiranek V (2016) Integrated strategies to moderate the alcohol content of wines. Wine Vitic J 31(5):33–38
Sadoudi M, Tourdot-Maréchal R, Rousseaux S, Steyer D, Gallardo-Chacón JJ, Ballester J, Vichi S, Guérin-Schneider R, Caixach J, Alexandre H (2012) Yeast–yeast interactions revealed by aromatic profile analysis of Sauvignon Blanc wine fermented by single or co-culture of non-Saccharomyces and Saccharomyces yeasts. Food Microbiol 32(2):243–253
Saerens SMG, Delvaux FR, Verstrepen KJ, Thevelein JM (2010) Production and biological function of volatile esters in Saccharomyces cerevisiae. Microb Biotechnol 3(2):165–177. https://doi.org/10.1111/j.1751-7915.2009.00106.x
Schwille P (2011) Bottom-up synthetic biology: engineering in a tinkerer’s world. Sci 333(6047):1252–1254. https://doi.org/10.1126/science.1211701
Siezen RJ (2008) Wine genomics. Microb Biotechnol 1(2):97–103. https://doi.org/10.1111/j.1751-7915.2008.00030.x
Singh R, Kumar M, Mittal A, Mehta PK (2016) Microbial enzymes: industrial progress in 21st century. Biotech 6(2):174–174. https://doi.org/10.1007/s13205-016-0485-8
Slavikova E, Vadkertiova R (2003) The diversity of yeasts in the agricultural soil. J Basic Microbiol 43(5):430–436. https://doi.org/10.1002/jobm.200310277
Snowdon EM, Bowyer MC, Grbin PR, Bowyer PK (2006) Mousy off-flavor: A review. J Ag Food Chem 54(18):6465-6474. https://doi.org/10.1021/jf0528613
Spitaels F, Wieme AD, Janssens M, Aerts M, Daniel H-M, Van Landschoot A, De Vuyst L, Vandamme P (2014) The microbial diversity of traditional spontaneously fermented lambic beer. PLoS One 9(4):e95384. https://doi.org/10.1371/journal.pone.0095384
Steensels J, Snoek T, Meersman E, Picca Nicolino M, Voordeckers K, Verstrepen KJ (2014a) Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol Rev 38(5):947–995. https://doi.org/10.1111/1574-6976.12073
Steensels J, Meersman E, Snoek T, Saels V, Verstrepen KJ (2014b) Large-scale selection and breeding to generate industrial yeasts with superior aroma production. Appl Environ Microbiol 80(22):6965–6975. https://doi.org/10.1128/AEM.02235-14
Stefanini I, Dapporto L, Legras J-L, Calabretta A, Di Paola M, De Filippo C, Viola R, Capretti P, Polsinelli M, Turillazzi S, Cavalieri D (2012) Role of social wasps in Saccharomycescerevisiae ecology and evolution. PNAS 109(33):13398–13403. https://doi.org/10.1073/pnas.1208362109
Sternes PR, Lee D, Kutyna DR, Borneman AR (2017) A combined meta-barcoding and shotgun metagenomic analysis of spontaneous wine fermentation. GigaScience 6(7):1–10. https://doi.org/10.1093/gigascience/gix040
Stewart G (2016) Saccharomyces species in the production of beer. Beverages 2(4):34
Sulaiman J, Gan HM, Yin WF, Chan KG (2014) Microbial succession and the functional potential during the fermentation of Chinese soy sauce brine. Front Microbiol 5:556. https://doi.org/10.3389/fmicb.2014.00556
Swiegers JH, Bartowsky EJ, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11(2):139–173. https://doi.org/10.1111/j.1755-0238.2005.tb00285.x
Szymanski EA (2018) Who are the users of synthetic DNA? Using metaphors to activate microorganisms at the center of synthetic biology. Life Sci Soc Policy 14(1):15. https://doi.org/10.1186/s40504-018-0080-3
Szymanski E, Calvert J (2018) Designing with living systems in the synthetic yeast project. Nat Commun 9(1):2950. https://doi.org/10.1038/s41467-018-05332-z
Tagliabue G (2016) The EU legislation on “GMOs” between nonsense and protectionism: an ongoing Schumpeterian chain of public choices. GM Crops Food 8(1):57–73. https://doi.org/10.1080/21645698.2016.1270488
Tamang JP, Watanabe K, Holzapfel WH (2016) Review: diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7:377–377. https://doi.org/10.3389/fmicb.2016.00377
Thurnell-Read T (2018) The embourgeoisement of beer: changing practices of ‘real ale’ consumption. J Consumer Culture 18(4):539–557. https://doi.org/10.1177/1469540516684189
Valles BS, Bedrinana RP, Tascon NF, Simon AQ, Madrera RR (2007) Yeast species associated with the spontaneous fermentation of cider. Food Microbiol 24(1):25–31. https://doi.org/10.1016/j.fm.2006.04.001
Varela C, Sengler F, Solomon M, Curtin C (2016) Volatile flavour profile of reduced alcohol wines fermented with the non-conventional yeast species Metschnikowia pulcherrima and Saccharomyces uvarum. Food Chem 209:57-64. https://doi.org/10.1016/j.foodchem.2016.04.024
Venetz JE, Del Medico L, Wölfle A, Schächle P, Bucher Y, Appert D, Tschan F, Flores-Tinoco CE, van Kooten M, Guennoun R, Deutsch S, Christen M, Christen B (2019) Chemical synthesis rewriting of a bacterial genome to achieve design flexibility and biological functionality. PNAS 116(16):8070–8079. https://doi.org/10.1073/pnas.1818259116
Viana F, Gil JV, Vallés S, Manzanares P (2009) Increasing the levels of 2-phenylethyl acetate in wine through the use of a mixed culture of Hanseniaspora osmophila and Saccharomyces cerevisiae. Int J Food Microbiol 135(1):68–74. https://doi.org/10.1016/j.ijfoodmicro.2009.07.025
Volschenk H, Viljoen M, Grobler J, Petzold B, Bauer F, Subden RE, Young RA, Lonvaud A, Denayrolles M, van Vuuren HJ (1997) Engineering pathways for malate degradation in Saccharomyces cerevisiae. Nat Biotech 15(3):253–257. https://doi.org/10.1038/nbt0397-253
Walker GM (2011) Pichia anomala: cell physiology and biotechnology relative to other yeasts. Ant van Leeuwenhoek 99(1):25–34. https://doi.org/10.1007/s10482-010-9491-8
Wunderlich S, Gatto KA (2015) Consumer perception of genetically modified organisms and sources of information. Adv Nutr 6(6):842–851. https://doi.org/10.3945/an.115.008870
Younis OS, Stewart GG (1998) Sugar uptake and subsequent ester and higher alcohol production by Saccharomyces cerevisiae. J Inst Brew 104(5):255–264. https://doi.org/10.1002/j.2050-0416.1998.tb00998.x
Zhang G-C, Kong II, Kim H, Liu JJ, Cate JHD, Jin Y-S (2014) Construction of a quadruple auxotrophic mutant of an industrial polyploid Saccharomyces cerevisiae strain by using RNA-guided Cas9 nuclease. Appl Environ Microbiol 80(24):7694–7701. https://doi.org/10.1128/aem.02310-14
Zhang XH, Tee LY, Wang XG, Huang QS, Yang SH (2015) Off-target effects in CRISPR/Cas9-mediated genome engineering. Molec Ther - Nuc Acids 4:e264. https://doi.org/10.1038/mtna.2015.37mixed
Acknowledgements
The University of Adelaide is a member of the Wine Innovation Cluster (http://www.thewaite.org.waite-partners/wine-innovation-cluster/).
Funding
This project was supported by funding from Wine Australia (UA1803-2.1) and The Australian Research Council Training Centre for Innovative Wine Production (www.ARCwinecentre.org.au; IC170100008), which is funded by the Australian Government with additional support from Wine Australia and industry partners. LA received a scholarship from the Playford Memorial Trust Inc.
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Alperstein, L., Gardner, J.M., Sundstrom, J.F. et al. Yeast bioprospecting versus synthetic biology—which is better for innovative beverage fermentation?. Appl Microbiol Biotechnol 104, 1939–1953 (2020). https://doi.org/10.1007/s00253-020-10364-x
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DOI: https://doi.org/10.1007/s00253-020-10364-x