Abstract
We used multilocus sequence typing (MLST) to analyze the diversity of natural isolates of Saccharomyces cerevisiae, the most important microorganism in alcoholic fermentation. Six loci, ADP1, RPN2, GLN4, ACC1, MET4, and NUP116, in S. cerevisiae genome were selected as MLST markers. To investigate genetic diversity within S. cerevisiae, 42 S. cerevisiae isolated from natural sources in Korea as well as six S. cerevisiae obtained from Genbank and four industrial S. cerevisiae were examined using MLST. Twenty-six polymorphic sites were found in the six loci. Among them, ACC1 had the most genetic variation with eight polymorphic sites. MLST differentiated the 52 strains into three clades. Alcohol fermentation results revealed that S. cerevisiae in Clade III produced less alcohol than those in Clades I and II. These results suggested that MLST is a powerful tool to differentiate S. cerevisiae and can potentially be used to select S. cerevisiae suitable for industrial use.
Similar content being viewed by others
References
Dalawai N, Krupa K, Nadkarni S, Bharani S, Harinikumar K. Screening of efficient ethanol tolerant yeast strain for production of ethanol. Int. J. Pure Appl. Biosci. 5: 744–752 (2017)
Novak J, Basarova G, Teixeira J, Vicente A. Monitoring of brewing yeast propagation under aerobic and anaerobic conditions employing flow cytometry. J. Inst. Brew. 113: 249–255 (2007)
Maslow JN, Mulligan ME, Arbeit RD. Molecular epidemiology: application of contemporary techniques to the typing of microorganisms. Clin. Infect. Dis. 17: 153–162 (1993)
Esteve-Zarzoso B, Hierro N, Mas A, Guillamón JM. A new simplified AFLP method for wine yeast strain typing. LWT Food Sci. Technol. 43: 1480–1484 (2010)
Muñoz R, Gómez A, Robles V, Rodríguez P, Cebollero E, Tabera L, Carrascosa AV, Gonzalez R. Multilocus sequence typing of oenological Saccharomyces cerevisiae strains. Food Microbiol. 26: 841–846 (2009)
Bidenne C, Blondin B, Dequin S, Vezinhet F. Analysis of the chromosomal DNA polymorphism of wine strains of Saccharomyces cerevisiae. Curr. Genet. 22: 1–7 (1992)
Grando MS, Ubeda J, Briones A. RAPD analysis of wine Saccharomyces cerevisiae strains differentiated by pulsed field gel electrophoresis. Biotechnol. Tech. 8: 557–560 (1994)
Masneuf I, Aigle M, Dubourdieu D. Development of a polymerase chain reaction/restriction fragment length polymorphism method for Saccharomyces cerevisiae and Saccharomyces bayanus identification in enology. FEMS Microbiol. Lett. 138: 239–244 (1996)
Guillamón JM, Barrio E. Genetic polymorphism in wine yeasts: mechanisms and methods for its detection. Front. Microbiol. 8: 1–20 (2017)
Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38: 1008–1015 (2000)
Sullivan CB, Diggle MA, Clarke SC. Multilocus sequence typing. Mol. Biotechnol. 29: 245 (2005)
Lee S, Yoo M, Shin D. The identification and quantification of biogenic amines in Korean turbid rice wine, Makgeolli by HPLC with mass spectrometry detection. LWT Food Sci. Technol. 62: 350–356 (2015)
Jung H, Lee S-J, Lim JH, Kim BK, Park KJ. Chemical and sensory profiles of Makgeolli, Korean commercial rice wine, from descriptive, chemical, and volatile compound analyses. Food Chem. 152: 624–632 (2014)
Jeong J-W, Nam P-W, Lee S-J, Lee K-G. Antioxidant activities of Korean rice wine concentrates. J. Agric. Food Chem. 59: 7039–7044 (2011)
Kang M-G, Kim J-H, Ahn B-H, Lee J-S. Characterization of new antihypertensive angiotensin I-converting enzyme inhibitory peptides from Korean traditional rice wine. J. Microbiol. Biotechnol. 22: 339–342 (2012)
Choi J-S, Seo HJ, Lee Y-R, Kwon S-J, Moon SH, Park S-M, Sohn JH. Characteristics and in vitro anti-diabetic properties of the Korean rice wine, makgeolli fermented with Laminaria japonica. Prev. Nutr. Food Sci. 19: 98 (2014)
Shin M-O, Kang D-Y, Kim M-H, Bae S-J. Effect of growth inhibition and quinone reductase activity stimulation of Makgeoly fractions in various cancer cells. J. Korean Soc. Food Sci. Nutr. 37: 288–293 (2008)
Jeon H, Yu JC, Kim G, Kong H-S. Quality characteristics of Takju by yeast strain type. Korean Soc. Food Sci. Nutr. 27: 971–978 (2014)
Baek SY, Lee YJ, Kim M-D, Yi J-H, Mun J-Y, Yeo S-H. Characterization of Ethanol fermentation with wild type yeast strains. Microbiol. Biotechnol. Lett. 43: 227–235 (2015)
Kang SH, Kim HR, Kim JH, Ahn BH, Kim TW, Lee J-E. Identification of wild yeast strains and analysis of their β-glucan and glutathione levels for use in Makgeolli brewing. Mycobiology 42: 361–367 (2014)
Mortimer RK, Johnston JR. Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35–43 (1986)
Carter DM, Liti G, Moses AM, Parts L, James SA, Davey RP, Roberts IN, Blomberg A, Warringer J, Burt A. Population genomics of domestic and wild yeasts. Nature 458: 337–341 (2008)
Akao T, Yashiro I, Hosoyama A, Kitagaki H, Horikawa H, Watanabe D, Akada R, Ando Y, Harashima S, Inoue T. Whole-genome sequencing of sake yeast Saccharomyces cerevisiae Kyokai no. 7. DNA Res. 18: 423–434 (2011)
Song G, Dickins BJ, Demeter J, Engel S, Dunn B, Cherry JM. AGAPE (Automated Genome Analysis PipelinE) for pan-genome analysis of Saccharomyces cerevisiae. PLoS ONE 10: e0120671 (2015)
Tavanti A, Davidson AD, Johnson EM, Maiden MC, Shaw DJ, Gow NA, Odds FC. Multilocus sequence typing for differentiation of strains of Candida tropicalis. J. Clin. Microbiol. 43: 5593–5600 (2005)
Tao G, Liu Z, Hyde K, Lui X, Yu Z. Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers. 33: 101–122 (2008)
Ayoub MJ, Legras JL, Saliba R, Gaillardin C. Application of multi locus sequence typing to the analysis of the biodiversity of indigenous Saccharomyces cerevisiae wine yeasts from Lebanon. J. Appl. Microbiol. 100: 699–711 (2006)
Pais FS-M, de Cássia Ruy P, Oliveira G, Coimbra RS. Assessing the efficiency of multiple sequence alignment programs. Algorithms Mol. Biol. 9: 4 (2014)
Tomasini N, Lauthier JJ, Llewellyn MS, Diosque P. MLSTest: Novel software for multi-locus sequence data analysis in eukaryotic organisms. Infect. Genet. Evol. 20: 188–196 (2013)
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425 (1987)
Woo K-S, Ko J-Y, Song S-B, Lee J-S, Oh B-G, Kang J-R, Nam M-H, Ryu I-S, Jeong H-S, Seo M-C. Physicochemical characteristics of Korean traditional wines prepared by addition of sorghum (Sorghum bicolor L. Moench) using different Nuruks. J. Korean Soc. Food Sci. Nutr. 39: 548–553 (2010)
Enright MC, Spratt BG. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144: 3049–3060 (1998)
Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Nati. Acad. Sci. 95: 3140–3145 (1998)
Dingle K, Colles F, Wareing D, Ure R, Fox A, Bolton F, Bootsma H, Willems R, Urwin R, Maiden M. Multilocus sequence typing system for Campylobacter jejuni. J. Clin. Microbiol. 39: 14–23 (2001)
Salcedo C, Arreaza L, Alcala B, De La Fuente L, Vazquez J. Development of a multilocus sequence typing method for analysis of Listeria monocytogenes clones. J. Clin. Microbiol. 41: 757–762 (2003)
Wu K, Luo T, Li L, Zhang Q, Zhu J, Gao Q, Chen M, Zhu M. Multilocus sequence typing of pathogenic Candida albicans isolates collected from a teaching hospital in Shanghai, China: a molecular epidemiology study. PLoS One 10: e0125245 (2015)
Acknowledgements
This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR201629202).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Eeom, YJ., Son, SY., Jung, DH. et al. Diversity analysis of Saccharomyces cerevisiae isolated from natural sources by multilocus sequence typing (MLST). Food Sci Biotechnol 27, 1119–1127 (2018). https://doi.org/10.1007/s10068-018-0335-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10068-018-0335-z