Abstract
Stress tolerance and resistance in industrial yeast strains are important attributes for cost-effective bioprocessing. The source of stress-tolerant yeasts ranges from extremophilic environments to laboratory engineered strains. However, industrial stress-tolerant yeasts are very rare in nature as the natural environment forces them to evolve traits that optimize survival and reproduction and not the ability to withstand harsh habitat-irrelevant industrial conditions. Experimental evolution is a frequent method used to uncover the mechanisms of evolution and microbial adaption towards environmental stresses. It optimizes biological systems by means of adaptation to environmental stresses and thus has immense power of development of robust stress-tolerant yeasts. This mini-review briefly outlines the basics and implications of evolution experiments and their applications to industrial biotechnology. This work is meant to serve as an introduction to those new to the field of experimental evolution, and as a guide to biologists working in the field of yeast stress response. Future perspectives of experimental evolution for potential biotechnological applications have also been elucidated.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams J, Rosenzweig F (2014) Experimental microbial evolution: history and conceptual underpinnings. Genomics 104(6 Pt A):393–398. https://doi.org/10.1016/j.ygeno.2014.10.004
Almeida MV, César Rosa J, Queirós H, Brandão R, Castro I (2014) Acid stress response in Saccharomyces cerevisiae involves ionic homeostasis and calcium signaling pathway. BMC Proc 8(Suppl 4):P193–P193. https://doi.org/10.1186/1753-6561-8-S4-P193
Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314(5805):1565–1568. https://doi.org/10.1126/science.1131969
Anderson JB, Sirjusingh C, Parsons AB, Boone C, Wickens C, Cowen LE, Kohn LM (2003) Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 163(4):1287–1298
Araya CL, Payen C, Dunham MJ, Fields S (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11:88. https://doi.org/10.1186/1471-2164-11-88
Attfield PV (1997) Stress tolerance: the key to effective strains of industrial baker's yeast. Nat Biotechnol 15(13):1351–1357. https://doi.org/10.1038/nbt1297-1351
Avrahami-Moyal L, Engelberg D, Wenger JW, Sherlock G, Braun S (2012) Turbidostat culture of Saccharomyces cerevisiae W303-1A under selective pressure elicited by ethanol selects for mutations in SSD1 and UTH1. FEMS Yeast Res 12(5):521–533. https://doi.org/10.1111/j.1567-1364.2012.00803.x
Barrick JE, Lenski RE (2013) Genome dynamics during experimental evolution. Nat Rev Genet 14(12):827–839. https://doi.org/10.1038/nrg3564
Beckner M, Ivey ML, Phister TG (2011) Microbial contamination of fuel ethanol fermentations. Lett Appl Microbiol 53(4):387–394. https://doi.org/10.1111/j.1472-765X.2011.03124.x
Behe MJ (2010) Experimental evolution, loss-of-function mutations, and “the first rule of adaptive evolution”. Q Rev Biol 85(4):419–445
Belda I, Ruiz J, Esteban-Fernandez A, Navascues E, Marquina D, Santos A, Moreno-Arribas MV (2017) Microbial contribution to wine aroma and its intended use for wine quality improvement. Molecules 22(2). https://doi.org/10.3390/molecules22020189
Bennett AF, Hughes BS (2009) Microbial experimental evolution. Am J Physiol Regul Integr Comp Physiol 297(1):R17–R25. https://doi.org/10.1152/ajpregu.90562.2008
Blundell JR, Levy SF (2014) Beyond genome sequencing: lineage tracking with barcodes to study the dynamics of evolution, infection, and cancer. Genomics 104(6 Pt A):417–430. https://doi.org/10.1016/j.ygeno.2014.09.005
Borodina I, Nielsen J (2014) Advances in metabolic engineering of yeast Saccharomyces cerevisiae for production of chemicals. Biotechnol J 9(5):609–620. https://doi.org/10.1002/biot.201300445
Bouws H, Wattenberg A, Zorn H (2008) Fungal secretomes—nature’s toolbox for white biotechnology. Appl Microbiol Biotechnol 80(3):381–388. https://doi.org/10.1007/s00253-008-1572-5
Boynton PJ, Greig D (2016) Fungal diversity and ecosystem function data from wine fermentation vats and microcosms. Data Brief 8:225–229. https://doi.org/10.1016/j.dib.2016.05.038
Boynton PJ, Stelkens R, Kowallik V, Greig D (2017) Measuring microbial fitness in a field reciprocal transplant experiment. Mol Ecol Resour 17(3):370–380. https://doi.org/10.1111/1755-0998.12562
Brewster JL, Gustin MC (2014) Hog1: 20 years of discovery and impact. Sci Signal 7(343):re7. https://doi.org/10.1126/scisignal.2005458
Broach JR (2012) Nutritional control of growth and development in yeast. Genetics 192(1):73–105. https://doi.org/10.1534/genetics.111.135731
Burke MK, Rose MR (2009) Experimental evolution with Drosophila. Am J Physiol Regul Integr Comp Physiol 296(6):R1847–R1854. https://doi.org/10.1152/ajpregu.90551.2008
Butler PR, Brown M, Oliver SG (1996) Improvement of antibiotic titers from Streptomyces bacteria by interactive continuous selection. Biotechnol Bioeng 49(2):185–196. https://doi.org/10.1002/(sici)1097-0290(19960120)49:2<185::aid-bit7>3.0.co;2-m
Cakar ZP, Alkim C, Turanli B, Tokman N, Akman S, Sarikaya M, Tamerler C, Benbadis L, François JM (2009) Isolation of cobalt hyper-resistant mutants of Saccharomyces cerevisiae by in vivo evolutionary engineering approach. J Biotechnol 143(2):130–138. https://doi.org/10.1016/j.jbiotec.2009.06.024
Cakar ZP, Seker UO, Tamerler C, Sonderegger M, Sauer U (2005) Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res 5(6-7):569–578. https://doi.org/10.1016/j.femsyr.2004.10.010
Caspeta L, Nielsen J (2015) Thermotolerant yeast strains adapted by laboratory evolution show trade-off at ancestral temperatures and preadaptation to other stresses. mBio 6(4):e00431. https://doi.org/10.1128/mBio.00431-15
Caspeta L, Chen Y, Ghiaci P, Feizi A, Buskov S, Hallström BM, Petranovic D, Nielsen J (2014) Altered sterol composition renders yeast thermotolerant. Science 346(6205):75–78
Charton C, Ulaszewski S, da Silva Vieira MR, Henoux V, Claisse ML (2004) Effects of oligomycins on adenosine triphosphatase activity of mitochondria isolated from the yeasts Saccharomyces cerevisiae and Schwanniomyces castellii. Biochem Biophys Res Commun 318(1):67–72. https://doi.org/10.1016/j.bbrc.2004.03.185
Chen Y, Stabryla L, Wei N (2016) Improved acetic acid resistance in Saccharomyces cerevisiae by overexpression of the WHI2 gene identified through inverse metabolic engineering. Appl Environ Microbiol 82(7):2156–2166. https://doi.org/10.1128/aem.03718-15
Chernin LS, De la Fuente L, Sobolev V, Haran S, Vorgias CE, Oppenheim AB, Chet I (1997) Molecular cloning, structural analysis, and expression in Escherichia coli of a chitinase gene from Enterobacter agglomerans. Appl Environ Microbiol 63(3):834–839
Conrad TM, Lewis NE, Palsson BO (2011) Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 7:509. https://doi.org/10.1038/msb.2011.42
Cordero-Bueso G, Mangieri N, Maghradze D, Foschino R, Valdetara F, Cantoral JM, Vigentini I (2017) Wild grape-associated yeasts as promising biocontrol agents against Vitis vinifera fungal pathogens. Front Microbiol 8:2025. https://doi.org/10.3389/fmicb.2017.02025
Cray JA, Stevenson A, Ball P, Bankar SB, Eleutherio ECA, Ezeji TC, Singhal RS, Thevelein JM, Timson DJ, Hallsworth JE (2015) Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Curr Opin Biotechnol 33:228–259. https://doi.org/10.1016/j.copbio.2015.02.010
Crowley S, Mahony J, van Sinderen D (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci Technol 33(2):93–109. https://doi.org/10.1016/j.tifs.2013.07.004
Dashko S, Zhou N, Compagno C, Piskur J (2014) Why, when, and how did yeast evolve alcoholic fermentation? FEMS Yeast Res 14(6):826–832. https://doi.org/10.1111/1567-1364.12161
Davidson JF, Whyte B, Bissinger PH, Schiestl RH (1996) Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93(10):5116–5121
Deparis Q, Claes A, Foulquie-Moreno MR, Thevelein JM (2017a) Engineering tolerance to industrially relevant stress factors in yeast cell factories. FEMS Yeast Res 17(4). https://doi.org/10.1093/femsyr/fox036
Deparis Q, Claes A, Foulquié-Moreno MR, Thevelein JM (2017b) Engineering tolerance to industrially relevant stress factors in yeast cell factories. FEMS Yeast Res 17(4):fox036. https://doi.org/10.1093/femsyr/fox036
Dhar R, SÄGesser R, Weikert C, Yuan J, Wagner A (2011) Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J Evol Biol 24(5):1135–1153. https://doi.org/10.1111/j.1420-9101.2011.02249.x
Dogan A, Demirci S, Aytekin AO, Sahin F (2014) Improvements of tolerance to stress conditions by genetic engineering in Saccharomyces cerevisiae during ethanol production. Appl Biochem Biotechnol 174(1):28–42. https://doi.org/10.1007/s12010-014-1006-z
Dragosits M, Mattanovich D (2013) Adaptive laboratory evolution -- principles and applications for biotechnology. Microb Cell Factories 12:64. https://doi.org/10.1186/1475-2859-12-64
Dunham MJ (2010a) Chapter 19 - experimental evolution in yeast: a practical guide methods in enzymology, vol 470. Academic Press, pp 487–507
Dunham MJ (2010b) Experimental evolution in yeast: a practical guide. Methods Enzymol 470:487–507. https://doi.org/10.1016/s0076-6879(10)70019-7
Dunham MJ (2012) Two flavors of bulk segregant analysis in yeast. Methods Mol Biol 871:41–54. https://doi.org/10.1007/978-1-61779-785-9_4
Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, Kroll E, Louis EJ, Liti G, Sherlock G, Rosenzweig F (2013) Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet 9(3):e1003366. https://doi.org/10.1371/journal.pgen.1003366
Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, Botstein D (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 99(25):16144–16149. https://doi.org/10.1073/pnas.242624799
Dykhuizen DE, Hartl DL (1983) Selection in chemostats. Microbiol Rev 47(2):150–168
Farwick A, Bruder S, Schadeweg V, Oreb M, Boles E (2014) Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc Natl Acad Sci U S A 111(14):5159–5164. https://doi.org/10.1073/pnas.1323464111
Ferea TL, Botstein D, Brown PO, Rosenzweig RF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci USA 96:9721–9726
Fischer CR, Klein-Marcuschamer D, Stephanopoulos G (2008) Selection and optimization of microbial hosts for biofuels production. Metab Eng 10(6):295–304. https://doi.org/10.1016/j.ymben.2008.06.009
Fletcher E, Krivoruchko A, Nielsen J (2016) Industrial systems biology and its impact on synthetic biology of yeast cell factories. Biotechnol Bioeng 113(6):1164–1170. https://doi.org/10.1002/bit.25870
Folch-Mallol JL, Garay-Arroyo A, Lledias F, Covarrubias Robles AA (2004) The stress response in the yeast Saccharomyces cerevisiae. Rev Latinoam Microbiol 46(1–2):24–46
Gallet R, Cooper TF, Elena SF, Lenormand T (2012) Measuring selection coefficients below 10(-3): method, questions, and prospects. Genetics 190(1):175–186. https://doi.org/10.1534/genetics.111.133454
Gancedo C, Flores CL (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4(4–5):351–359
Garland T Jr, Kelly SA (2006) Phenotypic plasticity and experimental evolution. J Exp Biol 209(Pt 12):2344–2361. https://doi.org/10.1242/jeb.02244
Ghiaci P, Norbeck J, Larsson C (2013) Physiological adaptations of Saccharomyces cerevisiae evolved for improved butanol tolerance. Biotechnol Biofuels 6:101–101. https://doi.org/10.1186/1754-6834-6-101
Gibson BR, Lawrence SJ, Leclaire JP, Powell CD, Smart KA (2007) Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol Rev 31(5):535–569. https://doi.org/10.1111/j.1574-6976.2007.00076.x
Gietz RD, Woods RA (2001) Genetic transformation of yeast. BioTechniques 30(4):816–820 822-6, 828 passim
Goddard MR (2008) Quantifying the complexities of Saccharomyces cerevisiae's ecosystem engineering via fermentation. Ecology 89(8):2077–2082
Gonzalez R, Morales P, Tronchoni J, Cordero-Bueso G, Vaudano E, Quirós M, Novo M, Torres-Pérez R, Valero E (2016) New genes involved in osmotic stress tolerance in Saccharomyces cerevisiae. Front Microbiol 7:1545. https://doi.org/10.3389/fmicb.2016.01545
González-Ramos D, Gorter de Vries AR, Grijseels SS, van Berkum MC, Swinnen S, van den Broek M, Nevoigt E, Daran JM, Pronk JT, van Maris AJ (2016) A new laboratory evolution approach to select for constitutive acetic acid tolerance in Saccharomyces cerevisiae and identification of causal mutations. Biotechnol Biofuels 9:173. https://doi.org/10.1186/s13068-016-0583-1
Gresham D, Dunham MJ (2014) The enduring utility of continuous culturing in experimental evolution. Genomics 104(6 Pt A):399–405. https://doi.org/10.1016/j.ygeno.2014.09.015
Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, Ward A, DeSevo CG, Botstein D, Dunham MJ (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4(12):e1000303. https://doi.org/10.1371/journal.pgen.1000303
Grubaugh ND, Smith DR, Brackney DE, Bosco-Lauth AM, Fauver JR, Campbell CL, Felix TA, Romo H, Duggal NK, Dietrich EA, Eike T, Beane JE, Bowen RA, Black WC, Brault AC, Ebel GD (2015) Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. PLoS Pathog 11(5):e1004874. https://doi.org/10.1371/journal.ppat.1004874
Hegde K, Chandra N, Sarma SJ, Brar SK, Veeranki VD (2015) Genetic engineering strategies for enhanced biodiesel production. Mol Biotechnol 57(7):606–624. https://doi.org/10.1007/s12033-015-9869-y
Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66(2):300–372
Hong J, Gresham D (2014) Molecular specificity, convergence and constraint shape adaptive evolution in nutrient-poor environments. PLoS Genet 10(1):e1004041. https://doi.org/10.1371/journal.pgen.1004041
Hong KK, Nielsen J (2012) Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries. Cell Mol Life Sci 69(16):2671–2690. https://doi.org/10.1007/s00018-012-0945-1
Hong KK, Nielsen J (2013) Adaptively evolved yeast mutants on galactose show trade-offs in carbon utilization on glucose. Metab Eng 16:78–86. https://doi.org/10.1016/j.ymben.2013.01.007
Hong KK, Vongsangnak W, Vemuri GN, Nielsen J (2011) Unravelling evolutionary strategies of yeast for improving galactose utilization through integrated systems level analysis. Proc Natl Acad Sci USA 108:12179–12184. https://doi.org/10.1073/pnas.1103219108
Huang CJ, Lu MY, Chang YW, Li WH (2018) Experimental evolution of yeast for high-temperature tolerance. Mol Biol Evol 35(8):1823–1839. https://doi.org/10.1093/molbev/msy077
Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR, Slade D, Burchard J, Dow S, Ward TR, Kidd MJ, Friend SH, Marton MJ (2000) Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 25(3):333–337. https://doi.org/10.1038/77116
Ishchuk OP, Voronovsky AY, Abbas CA, Sibirny AA (2009) Construction of Hansenula polymorpha strains with improved thermotolerance. Biotechnol Bioeng 104(5):911–919. https://doi.org/10.1002/bit.22457
Jansen ML, Daran-Lapujade P, De Winde JH, Piper MD, Pronk JT (2004) Prolonged maltose-limited cultivation of Saccharomyces cerevisiae selects for cells with improved maltose affinity and hypersensitivity. Appl Environ Microbiol 70:1956–1963. https://doi.org/10.1128/AEM.70.4.1956-1963.2004
Johnson EA, Echavarri-Erasun C (2011) Chapter 3 - yeast biotechnology A2 - Kurtzman, Cletus P. In: Fell JW, Boekhout T (eds) The yeasts, 5th edn. Elsevier, London, pp 21–44
Kao KC, Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40(12):1499–1504. https://doi.org/10.1038/Ng.280
Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC (2012) Experimental evolution. Trends Ecol Evol 27(10):547–560. https://doi.org/10.1016/j.tree.2012.06.001
Kelly SA, Czech PP, Wight JT, Blank KM, Garland T Jr (2006) Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice. J Morphol 267(3):360–374. https://doi.org/10.1002/jmor.10407
Kim IK, Roldao A, Siewers V, Nielsen J (2012) A systems-level approach for metabolic engineering of yeast cell factories. FEMS Yeast Res 12(2):228–248. https://doi.org/10.1111/j.1567-1364.2011.00779.x
Kinjo S, Monma N, Misu S, Kitamura N, Imoto J, Yoshitake K, Gojobori T, Ikeo K (2018) Maser: one-stop platform for NGS big data from analysis to visualization. Database (Oxford). https://doi.org/10.1093/database/bay027
Koppram R, Albers E, Olsson L (2012) Evolutionary engineering strategies to enhance tolerance of xylose utilizing recombinant yeast to inhibitors derived from spruce biomass. Biotechnol Biofuels 5(1):32. https://doi.org/10.1186/1754-6834-5-32
Krogerus K, Magalhaes F, Vidgren V, Gibson B (2017) Novel brewing yeast hybrids: creation and application. Appl Microbiol Biotechnol 101(1):65–78. https://doi.org/10.1007/s00253-016-8007-5
Kvitek DJ, Sherlock G (2013) Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet 9(11):e1003972. https://doi.org/10.1371/journal.pgen.1003972
Lambert RJ, Stratford M (1999) Weak-acid preservatives: modelling microbial inhibition and response. J Appl Microbiol 86(1):157–164
Lang GI, Desai MM (2014) The spectrum of adaptive mutations in experimental evolution. Genomics 104(6 Pt A):412–416. https://doi.org/10.1016/j.ygeno.2014.09.011
Lang GI, Botstein D, Desai MM (2011) Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 188(3):647–661. https://doi.org/10.1534/genetics.111.128942
Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, Desai MM (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500(7464):571–574. https://doi.org/10.1038/nature12344
Lenski RE (1998) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42(3):7. https://doi.org/10.2307/2409028
Lenski RE (2017) What is adaptation by natural selection? Perspectives of an experimental microbiologist. PLoS Genet 13(4):e1006668. https://doi.org/10.1371/journal.pgen.1006668
Levy SE, Myers RM (2016) Advancements in next-generation sequencing. Annu Rev Genomics Hum Genet 17(1):95–115. https://doi.org/10.1146/annurev-genom-083115-022413
Liu Z, Du S, Ren Y, Liu Y (2018) Biocontrol ability of killer yeasts (Saccharomyces cerevisiae) isolated from wine against Colletotrichum gloeosporioides on grape. J Basic Microbiol 58(1):60–67. https://doi.org/10.1002/jobm.201700264
Ludovico P, Sousa MJ, Silva MT, Leao C, Corte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147(Pt 9):2409–2415
Lutz MP, Wenger S, Maurhofer M, Defago G, Duffy B (2004) Signaling between bacterial and fungal biocontrol agents in a strain mixture. FEMS Microbiol Ecol 48(3):447–455. https://doi.org/10.1016/j.femsec.2004.03.002
Mans R, Daran JG, Pronk JT (2018) Under pressure: evolutionary engineering of yeast strains for improved performance in fuels and chemicals production. Curr Opin Biotechnol 50:47–56. https://doi.org/10.1016/j.copbio.2017.10.011
Marsit S, Dequin S (2015) Diversity and adaptive evolution of Saccharomyces wine yeast: a review. FEMS Yeast Res 15(7):fov067. https://doi.org/10.1093/femsyr/fov067
Mohd Azhar SH, Abdulla R, Jambo SA, Marbawi H, Gansau JA, Mohd Faik AA, Rodrigues KF (2017) Yeasts in sustainable bioethanol production: a review. Biochem Biophys Rep 10:52–61. https://doi.org/10.1016/j.bbrep.2017.03.003
Moktaduzzaman M, Galafassi S, Capusoni C, Vigentini I, Ling Z, Piskur J, Compagno C (2015) Galactose utilization sheds new light on sugar metabolism in the sequenced strain Dekkera bruxellensis CBS 2499. FEMS Yeast Res 15(2). https://doi.org/10.1093/femsyr/fou009
Morano KA, Grant CM, Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190(4):1157–1195. https://doi.org/10.1534/genetics.111.128033
Muzzey D, Gomez-Uribe CA, Mettetal JT, van Oudenaarden A (2009) A systems-level analysis of perfect adaptation in yeast osmoregulation. Cell 138(1):160–171. https://doi.org/10.1016/j.cell.2009.04.047
Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72(3):379–412. https://doi.org/10.1128/MMBR.00025-07
Nielsen J, Keasling Jay D (2016) Engineering cellular metabolism. Cell 164(6):1185–1197. https://doi.org/10.1016/j.cell.2016.02.004
Pais TM, Foulquie-Moreno MR, Hubmann G, Duitama J, Swinnen S, Goovaerts A, Yang Y, Dumortier F, Thevelein JM (2013) Comparative polygenic analysis of maximal ethanol accumulation capacity and tolerance to high ethanol levels of cell proliferation in yeast. PLoS Genet 9(6):e1003548. https://doi.org/10.1371/journal.pgen.1003548
Papadakis MA, Workman CT (2015) Oxidative stress response pathways: fission yeast as archetype. Crit Rev Microbiol 41(4):520–535. https://doi.org/10.3109/1040841x.2013.870968
Parrou JL, Jules M, Beltran G, Francois J (2005) Acid trehalase in yeasts and filamentous fungi: localization, regulation and physiological function. FEMS Yeast Res 5(6–7):503–511. https://doi.org/10.1016/j.femsyr.2005.01.002
Payen C, Sunshine AB, Ong GT, Pogachar JL, Zhao W, Dunham MJ (2016) High-throughput identification of adaptive mutations in experimentally evolved yeast populations. PLoS Genet 12(10):e1006339. https://doi.org/10.1371/journal.pgen.1006339
Pérez-Torrado R, Querol A, Guillamón JM (2015) Genetic improvement of non-GMO wine yeasts: strategies, advantages and safety. Trends Food Sci Technol 45(1):1–11. https://doi.org/10.1016/j.tifs.2015.05.002
Petti AA, Crutchfield CA, Rabinowitz JD, Botstein D (2011) Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function. Proc Natl Acad Sci U S A 108(45):E1089–E1098. https://doi.org/10.1073/pnas.1101494108
Piotrowski JS, Nagarajan S, Kroll E, Stanbery A, Chiotti KE, Kruckeberg AL, Dunn B, Sherlock G, Rosenzweig F (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evol Biol 12:46. https://doi.org/10.1186/1471-2148-12-46
Portnoy VA, Bezdan D, Zengler K (2011) Adaptive laboratory evolution--harnessing the power of biology for metabolic engineering. Curr Opin Biotechnol 22(4):590–594. https://doi.org/10.1016/j.copbio.2011.03.007
Querol A, Fernández-Espinar MT, del Olmo ML, Amp X, Barrio E (2003) Adaptive evolution of wine yeast. Int J Food Microbiol 86(1–2):3–10. https://doi.org/10.1016/S0168-1605(03)00244-7
Raveendran S, Parameswaran B, Ummalyma SB, Abraham A, Mathew AK, Madhavan A, Rebello S, Pandey A (2018) Applications of microbial enzymes in food industry. Food Technol Biotechnol 56(1):16–30. https://doi.org/10.17113/ftb.56.01.18.5491
Reed G, Nagodawithana T (1990) Baker’s yeast production yeast technology. Springer, Netherlands, pp 261–314
Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192(2):289–318. https://doi.org/10.1534/genetics.112.140863
Samani P, Bell G (2016) Experimental evolution of the grain of metabolic specialization in yeast. Ecol Evol 6(12):3912–3922. https://doi.org/10.1002/ece3.2151
Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Engin/Biotechnol 73:129–169
Selmecki AM, Dulmage K, Cowen LE, Anderson JB, Berman J (2009) Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet 5(10):e1000705. https://doi.org/10.1371/journal.pgen.1000705
Serra-Cardona A, Canadell D, Ariño J (2015) Coordinate responses to alkaline pH stress in budding yeast. Microb Cell 2(6):182–196. https://doi.org/10.15698/mic2015.06.205
Smukowski Heil CS, DeSevo CG, Pai DA, Tucker CM, Hoang ML, Dunham MJ (2017) Loss of heterozygosity drives adaptation in hybrid yeast. Mol Biol Evol 34(7):1596–1612. https://doi.org/10.1093/molbev/msx098
St Leger RJ, Wang C (2010) Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl Microbiol Biotechnol 85(4):901–907. https://doi.org/10.1007/s00253-009-2306-z
Steensels J, Snoek T, Meersman E, Picca Nicolino M, Voordeckers K, Verstrepen KJ (2014) Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol Rev 38(5):947–995. https://doi.org/10.1111/1574-6976.12073
Stovicek V, Borodina I, Forster J (2015) CRISPR–Cas system enables fast and simple genome editing of industrial Saccharomyces cerevisiae strains. Metab Eng 2:13–22. https://doi.org/10.1016/j.meteno.2015.03.001
Stovicek V, Holkenbrink C, Borodina I (2017) CRISPR/Cas system for yeast genome engineering: advances and applications. FEMS Yeast Res 17(5). https://doi.org/10.1093/femsyr/fox030
Sui Y, Wisniewski M, Droby S, Liu J (2015) Responses of yeast biocontrol agents to environmental stress. Appl Environ Microbiol 81(9):2968–2975. https://doi.org/10.1128/AEM.04203-14
Szamecz B, Boross G, Kalapis D, Kovacs K, Fekete G, Farkas Z, Lazar V, Hrtyan M, Kemmeren P, Groot Koerkamp MJ, Rutkai E, Holstege FC, Papp B, Pal C (2014) The genomic landscape of compensatory evolution. PLoS Biol 12(8):e1001935. https://doi.org/10.1371/journal.pbio.1001935
Tesfaw A, Assefa F (2014) Current trends in bioethanol production by Saccharomyces cerevisiae: substrate, inhibitor reduction, growth variables, coculture, and immobilization. Int Sch Res Notices 2014:532852–532811. https://doi.org/10.1155/2014/532852
Tilloy V, Ortiz-Julien A, Dequin S (2014) Reduction of ethanol yield and improvement of glycerol formation by adaptive evolution of the wine yeast Saccharomyces cerevisiae under hyperosmotic conditions. Appl Environ Microbiol 80(8):2623–2632. https://doi.org/10.1128/AEM.03710-13
Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128(4):1271–1281. https://doi.org/10.1104/pp.010999
Van den Bergh B, Swings T, Fauvart M, Michiels J (2018) Experimental design, population dynamics, and diversity in microbial experimental evolution. Microbiol Mol Biol Rev 82(3). https://doi.org/10.1128/MMBR.00008-18
Vasi F, Travisano M, Lenski RE (1994) Long-term experimental evolution in Escherichia coli. II. changes in life-history traits during adaptation to a seasonal environment. Am Nat 144(3):432–456. https://doi.org/10.1086/285685
Velmeshev D, Lally P, Magistri M, Faghihi MA (2016) CANEapp: a user-friendly application for automated next generation transcriptomic data analysis. BMC Genomics 17:49. https://doi.org/10.1186/s12864-015-2346-y
Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76(2):115–158. https://doi.org/10.1128/MMBR.05018-11
Voordeckers K, Verstrepen KJ (2015) Experimental evolution of the model eukaryote Saccharomyces cerevisiae yields insight into the molecular mechanisms underlying adaptation. Curr Opin Microbiol 28:1–9. https://doi.org/10.1016/j.mib.2015.06.018
Voordeckers K, Kominek J, Das A, Espinosa-Cantu A, De Maeyer D, Arslan A, Van Pee M, van der Zande E, Meert W, Yang Y, Zhu B, Marchal K, DeLuna A, Van Noort V, Jelier R, Verstrepen KJ (2015) Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet 11(11):e1005635. https://doi.org/10.1371/journal.pgen.1005635
Walker GM (1998) Yeast physiology and biotechnology
Wallace-Salinas V, Gorwa-Grauslund MF (2013) Adaptive evolution of an industrial strain of Saccharomyces cerevisiae for combined tolerance to inhibitors and temperature. Biotechnol Biofuels 6(1):151. https://doi.org/10.1186/1754-6834-6-151
Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, Rosenzweig F (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7(8):e1002202. https://doi.org/10.1371/journal.pgen.1002202
Winkler JD, Kao KC (2014) Recent advances in the evolutionary engineering of industrial biocatalysts. Genomics 104(6 Pt A):406–411. https://doi.org/10.1016/j.ygeno.2014.09.006
Wright J, Bellissimi E, de Hulster E, Wagner A, Pronk JT, van Maris AJ (2011) Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae. FEMS Yeast Res 11(3):299–306. https://doi.org/10.1111/j.1567-1364.2011.00719.x
Yokota M, Fagerson IS (1971) The major volatile components of cane molasses. J Food Sci 36(7):1091–1094. https://doi.org/10.1111/j.1365-2621.1971.tb03353.x
Zelle RM, Trueheart J, Harrison JC, Pronk JT, Van Maris AJ (2010) Phosphoenolpyruvate carboxykinase as the sole anaplerotic enzyme in Saccharomyces cerevisiae. Appl Environ Microbiol 76:5383–5389. https://doi.org/10.1128/AEM.01077-10
Zeyl C (2004) Experimental studies on ploidy evolution in yeast. FEMS Microbiol Lett 233(2):187–192
Zeyl C (2006) Experimental evolution with yeast. Fems Yeast Res 6(5):685–691. https://doi.org/10.1111/J.1567-1364.2006.00061.X
Zeyl C, Curtin C, Karnap K, Beauchamp E (2005) Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae. Evolution 59(10):2109–2115
Zhang N, Cao L (2017) Starvation signals in yeast are integrated to coordinate metabolic reprogramming and stress response to ensure longevity. Curr Genet 63(5):839–843. https://doi.org/10.1007/s00294-017-0697-4
Zhao L, Liu Z, Levy SF, Wu S (2018) Bartender: a fast and accurate clustering algorithm to count barcode reads. Bioinformatics 34(5):739–747. https://doi.org/10.1093/bioinformatics/btx655
Zhou N, Bottagisi S, Katz M, Schacherer J, Friedrich A, Gojkovic Z, Swamy KBS, Knecht W, Compagno C, Piskur J (2017) Yeast-bacteria competition induced new metabolic traits through large-scale genomic rearrangements in Lachancea kluyveri. FEMS Yeast Res 17(6). https://doi.org/10.1093/femsyr/fox060
Zhou N, Swamy KB, Leu JY, McDonald MJ, Galafassi S, Compagno C, Piskur J (2017) Coevolution with bacteria drives the evolution of aerobic fermentation in Lachancea kluyveri. PLoS One 12(3):e0173318. https://doi.org/10.1371/journal.pone.0173318
Zhou N, Katz M, Knecht W, Compagno C, Piskur J (2018) Genome dynamics and evolution in yeasts: a long-term yeast-bacteria competition experiment. PLoS One 13(4):e0194911. https://doi.org/10.1371/journal.pone.0194911
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure declaration and ethical statement
The authors declare that there are no conflicts of interest. The strains mentioned in this mini-review are available in public databases. The articles mentioned in this work are in accordance with ethical standards.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Swamy, K.B.S., Zhou, N. Experimental evolution: its principles and applications in developing stress-tolerant yeasts. Appl Microbiol Biotechnol 103, 2067–2077 (2019). https://doi.org/10.1007/s00253-019-09616-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-09616-2