Abstract
Yeasts are a diverse seemingly ubiquitous group of eukaryotic microbes, and many are naturally associated with fruits. Humans have harnessed yeasts since the dawn of civilisation to make wine, and thus it is surprising that we know little of the distribution of yeast communities naturally associated with fruits. Previous reports of yeast community diversity have been descriptive only. Here we present, we believe, the first robust test for the geographic delineation of yeast communities. Humans have relatively recently employed Saccharomyces cerevisiae as a model research organism, and have long harnessed its ancient adaption to ferment even in the presence of oxygen. However, as far as we are aware, there has not been a rigorous test for the presence of regional differences in natural S. cerevisiae populations before. We combined these community- and population-level questions and surveyed replicate vineyards and corresponding spontaneous ferments from different regions on New Zealand's (NZ's) North Island and analysed the resulting data with community ecology and population genetic tests. We show that there are distinct regional delineations of yeast communities, but the picture for S. cerevisiae is more complex: there is evidence for region-specific sub-populations but there are also reasonable levels of gene flow among these regions in NZ. We believe this is the first demonstration of regional delineations of yeast populations and communities worldwide.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Anfang N, Brajkovich M, Goddard MR . (2009). Co-fermentation with Pichia kluyveri increases varietal thiol concentrations in Sauvignon Blanc. Aust J Grape Wine R 15: 1–8.
Beltran G, Torija MJ, Novo M, Ferrer N, Poblet M, Guillamon JM et al. (2002). Analysis of yeast populations during alcoholic fermentation: a six year follow-up study. Syst Appl Microbiol 25: 287–293.
Blanco P, Orriols I, Losada A . (2011). Survival of commercial yeasts in the winery environment and their prevalence during spontaneous fermentations. J Ind Microbiol Biot 38: 235–239.
Burke D, Dawson D, Stearns T . (2000). Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Press: Cold Spring Harbor.
Cadez N, Zupan J, Raspor P . (2010). The effect of fungicides on yeast communities associated with grape berries. FEMS Yeast Res 10: 619–630.
Chambers PJ, Pretorius IS . (2010). Fermenting knowledge: the history of winemaking, science and yeast research. EMBO Rep 11: 914–920.
Ciani M, Comitini F, Mannazzu I, Domizio P . (2010). Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10: 123–133.
Clarke KR . (1993). Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143.
Cordente AG, Swiegers JH, Hegardt FG, Pretorius IS . (2007). Modulating aroma compounds during wine fermentation by manipulating carnitine acetyltransferases in Saccharomyces cerevisiae. FEMS Microbiol Lett 267: 159–166.
Cordero-Bueso G, Arroyo T, Serrano A, Tello J, Aporta I, Velez MD et al. (2011). Influence of the farming system and vine variety on yeast communities associated with grape berries. Intl J Food Micro 145: 132–139.
Cox CB, Moore PD . (1993). Biogeography, an Ecological and Evolutionary Approach. Blackwell: London.
Cubillos FA, Vasquez C, Faugeron S, Ganga A, Martinez C . (2009). Self-fertilization is the main sexual reproduction mechanism in native wine yeast populations. FEMS Microbiol Ecol 67: 162–170.
Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R et al. (2011). Geneious v5.4, Available from http://www.geneious.com/.
Dujon B . (1996). The yeast genome project: what did we learn? Trends Genet 12: 263–270.
Esteve-Zarzoso B, Belloch C, Uruburu F, Querol A . (1999). Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. Int J Syst Bacteriol 49: 329–337.
Ezov TK, Boger-Nadjar E, Frenkel Z, Katsperovski I, Kemeny S, Nevo E et al. (2006). Molecular-genetic biodiversity in a natural population of the yeast Saccharomyces cerevisiae from ‘Evolution canyon’: microsatellite polymorphism, ploidy and controversial sexual status. Genetics 174: 1455–1468.
Falconer DS, Mackay TFC . (1996). Introduction to Quantitative Genetics, 4th edn. Pearson, Prentice Hall: New Jersey.
Falush D, Stephens M, Pritchard JK . (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.
Fay JC, Benavides JA . (2005). Evidence for domesticated and wild populations of Sacchoromyces cerevisiae. PLOS Genetics 1: 66–71.
Finlay BJ, Fenchel T . (2004). Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist 155: 237–244.
Gao H, Williamson S, Bustamante CD . (2007). A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176: 1635–1651.
Gaston KJ . (2000). Global patterns in biodiversity. Nature 405: 220–227.
Goddard MR . (2008). Quantifying the complexities of Saccharomyces cerevisiae′s ecosystem engineering via fermentation. Ecology 89: 2077–2082.
Goddard MR, Anfang N, Tang R, Gardner RC, Jun C . (2010). A distinct population of Saccharomyces cerevisiae in New Zealand: evidence for local dispersal by insects and human-aided global dispersal in oak barrels. Environ Microbiol 12: 63–73.
Goddard MR, Greig D, Burt A . (2001). Outcrossed sex allows a selfish gene to invade yeast populations. Proc R Soc Lond B-Biol Sci 268: 2537–2542.
Goode J . (2006). The Science of Wine. University of California Press: Berkeley.
Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M et al. (2004). Spatial scaling of microbial eukaryote diversity. Nature 432: 747–750.
Hamamoto M, Nakase T . (1996). Ballistosporous yeasts found on the surface of plant materials collected in New Zealand—the genera Bensingtonia and Bullera with descriptions of five new species. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 69: 279–291.
Hammer O, Harper DAT, Ryan PD . (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4 art. 4: 9 pp. (online only http://palaeo-electronica.org/2001_1/past/issue1_01.htm).
Hartl DL, Clark AG . (1997). Principles of Population Genetics, 3rd edn. Sinauer: Sunderland.
Howell KS, Cozzolino D, Bartowsky EJ, Fleet GH, Henschke PA . (2006). Metabolic profiling as a tool for revealing Saccharomyces interactions during wine fermentation. FEMS Yeast Res 6: 91–101.
Huelsenbeck JP, Andolfatto P . (2007). Inference of population structure under a Dirichlet process model. Genetics 175: 1787–1802.
Hugenholtz P, Goebel BM, Pace NR . (1998). Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765–4774.
Johnson H . (1998). The Story of Wine. Simon and Schuster: London.
Johnson LJ, Koufopanou V, Goddard MR, Hetherington R, Schafer SM, Burt A . (2004). Population genetics of the wild yeast Saccharomyces paradoxus. Genetics 166: 43–52.
Kalinowski ST . (2005). HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5: 187–189.
King ES, Kievit RL, Curtin C, Swiegers JH, Pretorius IS, Bastian SEP et al. (2010). The effect of multiple yeasts co-inoculations on Sauvignon Blanc wine aroma composition, sensory properties and consumer preference. Food Chem 122: 618–626.
King M . (2003). History of New Zealand. Penguin: Auckland.
Knop M . (2006). Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding. Bioessays 28: 696–708.
Koufopanou V, Hughes J, Bell G, Burt A . (2006). The spatial scale of genetic differentiation in a model organism: the wild yeast Saccharomyces paradoxus. Philos T R Soc B 361: 1941–1946.
Kurtzman CP, Robnett CJ . (2003). Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Res 3: 417–432.
Lachance MA, Lawrie D, Dobson J, Piggott J . (2008). Biogeography and population structure of the Neotropical endemic yeast species Metschnikowia lochheadii. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 94: 403–414.
Lachance MA, Starmer WT, Bowles JM, Phaff HJ, Rosa CA . (2000). Ribosomal DNA, species structure, and biogeography of the cactophilic yeast Clavispora opuntiae. Can J Microbiol 46: 195–210.
Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH . (2001). Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1: 1–8.
Lambrechts MG, Pretorius IS . (2000). Yeast and its importance to wine aroma—a review. S Afr J Enol Vitic 21: 97–129.
Landry CR, Townsend JP, Hartl DL, Cavalieri D . (2006). Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15: 575–591.
Legras JL, Merdinoglu D, Cornuet JM, Karst F . (2007). Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16: 2091–2102.
Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA et al. (2009). Population genomics of domestic and wild yeasts. Nature 458: 337–341.
Martinez C, Cosgaya P, Vasquez C, Gac S, Ganga A . (2007). High degree of correlation between molecular polymorphism and geographic origin of wine yeast strains. J Appl Microbiol 103: 2185–2195.
Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4: 102–112.
McGovern PE, Zhang J, Tang J, Zhang Z, Hall GR, Moreau RA et al. (2004). Fermented beverages of pre- and proto-historic China. Proc Natl Acad Sci USA 101: 17593–17598.
Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, Schmidt SK et al. (2011). Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13: 135–144.
Peakall R, Smouse PE . (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288–295.
Pedros-Alio C . (2007). Dipping into the rare biosphere. Science 315: 192–193.
Piskur J, Rozpedowska E, Polakova S, Merico A, Compagno C . (2006). How did Saccharomyces evolve to become a good brewer? Trends Genet 22: 183–186.
Prakitchaiwattana CJ, Fleet GH, Heard GM . (2004). Application and evaluation of denaturing gradient gel electrophoresis to analyse the yeast ecology of wine grapes. FEMS Yeast Res 4: 865–877.
Pretorius IS . (2000). Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16: 675–729.
Replansky T, Koufopanou V, Greig D, Bell G . (2008). Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol Evol 23: 494–501.
Ribereau-Gayon P, Dobourdieu D, Doneche B, Lonvaud A . (2006). Handbook of Enology, Vol. 1 The Microbiology of Wine and Vinifications. John Wiley & Sons, Ltd: Chichetser, UK.
Richards KD, Goddard MR, Gardner RC . (2009). A database of microsatellite genotypes for Saccharomyces cerevisiae. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 96: 355–359.
Romano P, Fiore C, Paraggio M, Caruso M, Capece A . (2003). Function of yeast species and strains in wine flavour. Intl J Food Micro 86: 169–180.
Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L . (2009). Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342–345.
Schuller D, Alves H, Dequin S, Casal M . (2005). Ecological survey of Saccharomyces cerevisiae strains from vineyards in the Vinho Verde Region of Portugal. FEMS Microbiol Ecol 51: 167–177.
Schuller D, Casal M . (2007). The genetic structure of fermentative vineyard-associated Saccharomyces cerevisiae populations revealed by microsatellite analysis. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 91: 137–150.
Serjeant K, Tang R, Anfang N, Beggs JR, Goddard MR . (2008). Yeasts associated with the New Zealand Nothofagus honeydew system. New Zeal J Ecol 32: 209–213.
Swiegers JH, Pretorius IS . (2005). Yeast modulation of wine flavor. Adv Appl Microbiol 57: 131–175.
Swiegers JH, Pretorius IS . (2007). Modulation of volatile sulfur compounds by wine yeast. Appl Microbiol Biotechnol 74: 954–960.
Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP et al. (2005). Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37: 630–635.
Whitaker RJ, Grogan DW, Taylor JW . (2003). Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301: 976–978.
Wolfe KH, Shields DC . (1997). Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708–713.
Zhang HY, Lee SA, Bradbury JE, Warren RN, Seth H, Hooks D et al. (2010a). Yeasts isolated from New Zealand vineyards and wineries. Aust J Grape Wine R 16: 491–496.
Zhang HY, Skelton A, Gardner RC, Goddard MR . (2010b). Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids. FEMS Yeast Res 10: 941–947.
Acknowledgements
We thank Michael Brajkovich MW at Kumeu River Wines, Pernod-Ricard NZ (especially Tony Robb), Waiheke Winegrowers (Obsidian, Mudbrick, Kennedy Point), Trinity Hill, and Mission Estate for their support and involvement with this project. We also thank the anonymous reviewers for comments on drafts of this paper. This work was directly supported by a Faculty Research grant to MG, but is part of a larger research program supported by New Zealand Winegrowers and the Ministry for Science and Innovation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website
Rights and permissions
About this article
Cite this article
Gayevskiy, V., Goddard, M. Geographic delineations of yeast communities and populations associated with vines and wines in New Zealand. ISME J 6, 1281–1290 (2012). https://doi.org/10.1038/ismej.2011.195
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2011.195
Keywords
This article is cited by
-
The relative abundances of yeasts attractive to Drosophila suzukii differ between fruit types and are greatest on raspberries
Scientific Reports (2022)
-
Separate and combined Hanseniaspora uvarum and Metschnikowia pulcherrima metabolic volatiles are attractive to Drosophila suzukii in the laboratory and field
Scientific Reports (2021)
-
Biodiversity of non-Saccharomyces yeasts associated with spontaneous fermentation of Cabernet Sauvignon wines from Shangri-La wine region, China
Scientific Reports (2021)
-
Microscale analysis of soil characteristics and microbiomes reveals potential impacts on plants and fruit: vineyard as a model case study
Plant and Soil (2021)
-
Quantifying the effect of human practices on S. cerevisiae vineyard metapopulation diversity
Scientific Reports (2020)