Summer temperature can predict the distribution of wild yeast populations

Abstract The wine yeast, Saccharomyces cerevisiae, is the best understood microbial eukaryote at the molecular and cellular level, yet its natural geographic distribution is unknown. Here we report the results of a field survey for S. cerevisiae,S. paradoxus and other budding yeast on oak trees in Europe. We show that yeast species differ in their geographic distributions, and investigated which ecological variables can predict the isolation rate of S. paradoxus, the most abundant species. We find a positive association between trunk girth and S. paradoxus abundance suggesting that older trees harbor more yeast. S. paradoxus isolation frequency is also associated with summer temperature, showing highest isolation rates at intermediate temperatures. Using our statistical model, we estimated a range of summer temperatures at which we expect high S. paradoxus isolation rates, and show that the geographic distribution predicted by this optimum temperature range is consistent with the worldwide distribution of sites where S. paradoxus has been isolated. Using laboratory estimates of optimal growth temperatures for S. cerevisiae relative to S. paradoxus, we also estimated an optimum range of summer temperatures for S. cerevisiae. The geographic distribution of these optimum temperatures is consistent with the locations where wild S. cerevisiae have been reported, and can explain why only human‐associated S. cerevisiae strains are isolated at northernmost latitudes. Our results provide a starting point for targeted isolation of S. cerevisiae from natural habitats, which could lead to a better understanding of climate associations and natural history in this important model microbe.

[1]  Nellie Clarke Brown Trees , 1896, Savage Dreams.

[2]  D. Ellis,et al.  The Yeasts , 1921, Nature.

[3]  S. Schor STATISTICS: AN INTRODUCTION. , 1965, The Journal of trauma.

[4]  J. Bonfield,et al.  A new DNA sequence assembly program. , 1995, Nucleic acids research.

[5]  P. Sniegowski,et al.  Differentiation of European and Far East Asian populations of Saccharomyces paradoxus by allozyme analysis. , 1997, International journal of systematic bacteriology.

[6]  K. Rushforth Trees of Britain and Europe , 1999 .

[7]  P. Sniegowski,et al.  Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. , 2002, FEMS yeast research.

[8]  A. Burt,et al.  Population Genetics of the Wild Yeast Saccharomyces paradoxus , 2004, Genetics.

[9]  P. Sniegowski,et al.  Sympatric natural Saccharomyces cerevisiae and S. paradoxus populations have different thermal growth profiles. , 2004, FEMS yeast research.

[10]  Y. Bar-Yam,et al.  Estimating the total genetic diversity of a spatial field population from a sample and implications of its dependence on habitat area. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Thevelein,et al.  Aquaporin Expression and Freeze Tolerance in Candida albicans , 2005, Applied and Environmental Microbiology.

[12]  W. Bowman,et al.  A temporal approach to linking aboveground and belowground ecology. , 2005, Trends in ecology & evolution.

[13]  Justin C. Fay,et al.  Evidence for Domesticated and Wild Populations of Saccharomyces cerevisiae , 2005, PLoS genetics.

[14]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[15]  J. Schnürer,et al.  Biotechnology, physiology and genetics of the yeast Pichia anomala. , 2006, FEMS yeast research.

[16]  J. Townsend,et al.  Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  James H. Brown,et al.  Microbial biogeography: putting microorganisms on the map , 2006, Nature Reviews Microbiology.

[18]  C. Rosa,et al.  Biodiversity and ecophysiology of yeasts , 2006 .

[19]  Hon Keung Tony Ng,et al.  Statistics: An Introduction Using R , 2006, Technometrics.

[20]  T. Deák Environmental Factors Influencing Yeasts , 2006 .

[21]  J. Stalpers,et al.  Yeast biodiversity and culture collections , 2006 .

[22]  B. Bohannan,et al.  Spatial scaling of microbial biodiversity. , 2006, Trends in ecology & evolution.

[23]  P. Sniegowski,et al.  Allopatric Divergence, Secondary Contact, and Genetic Isolation in Wild Yeast Populations , 2007, Current Biology.

[24]  A. M. Glushakova,et al.  Massive isolation and identification of Saccharomyces paradoxus yeasts from plant phyllosphere , 2007, Microbiology.

[25]  P. Palange,et al.  From the authors , 2007, European Respiratory Journal.

[26]  E. Sláviková,et al.  Yeasts colonizing the leaf surfaces , 2007, Journal of basic microbiology.

[27]  Leopold Parts,et al.  Population genomics of domestic and wild yeasts , 2008 .

[28]  P. Gonçalves,et al.  Natural Populations of Saccharomyces kudriavzevii in Portugal Are Associated with Oak Bark and Are Sympatric with S. cerevisiae and S. paradoxus , 2008, Applied and Environmental Microbiology.

[29]  A. Burt,et al.  Rapid Evolution of Yeast Centromeres in the Absence of Drive , 2008, Genetics.

[30]  M. Usher The Biology of Soil: A Community and Ecosystem Approach , 2008 .

[31]  Robert P. Davey,et al.  Population genomics of domestic and wild yeasts , 2008, Nature.

[32]  F. Dietrich,et al.  Saccharomyces cerevisiae: Population Divergence and Resistance to Oxidative Stress in Clinical, Domesticated and Wild Isolates , 2009, PloS one.

[33]  Rongying Tang,et al.  A distinct population of Saccharomyces cerevisiae in New Zealand: evidence for local dispersal by insects and human-aided global dispersal in oak barrels. , 2010, Environmental microbiology.

[34]  M. Goddard,et al.  Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids. , 2010, FEMS yeast research.

[35]  Justin C. Fay,et al.  Incipient Balancing Selection through Adaptive Loss of Aquaporins in Natural Saccharomyces cerevisiae Populations , 2010, PLoS genetics.

[36]  D. Bensasson Evidence for a high mutation rate at rapidly evolving yeast centromeres , 2011, BMC Evolutionary Biology.

[37]  C. Kurtzman Wickerhamomyces Kurtzman, Robnett & Basehoar-Powers (2008) , 2011 .

[38]  M. Lachance,et al.  Lachancea Kurtzman (2003) , 2011 .

[39]  Z. Salvadó,et al.  Temperature Adaptation Markedly Determines Evolution within the Genus Saccharomyces , 2011, Applied and Environmental Microbiology.

[40]  C. Kurtzman,et al.  Candida Berkhout (1923) , 2011 .

[41]  G. Liti,et al.  Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity , 2012, Molecular ecology.

[42]  Jianping Xu,et al.  Ecological structuring of yeasts associated with trees around Hamilton, Ontario, Canada. , 2012, FEMS yeast research.

[43]  M. Araújo,et al.  Uses and misuses of bioclimatic envelope modeling. , 2012, Ecology.

[44]  Justin C. Fay,et al.  Mixing of vineyard and oak‐tree ecotypes of Saccharomyces cerevisiae in North American vineyards , 2013, Molecular ecology.

[45]  Justin C. Fay,et al.  Genomic Sequence Diversity and Population Structure of Saccharomyces cerevisiae Assessed by RAD-seq , 2013, G3: Genes, Genomes, Genetics.

[46]  A. Friedrich,et al.  Population Genomic Analysis Reveals Highly Conserved Mitochondrial Genomes in the Yeast Species Lachancea thermotolerans , 2014, Genome biology and evolution.

[47]  D. Greig,et al.  The ecology and evolution of non-domesticated Saccharomyces species , 2014, Yeast.

[48]  Jean-Baptiste Leducq,et al.  Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. , 2014, FEMS yeast research.

[49]  G. Bell,et al.  Local climatic adaptation in a widespread microorganism , 2014, Proceedings of the Royal Society B: Biological Sciences.

[50]  C. T. Hittinger,et al.  Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species. , 2015, FEMS yeast research.

[51]  D. Greig,et al.  Saccharomyces cerevisiae: a nomadic yeast with no niche? , 2015, FEMS yeast research.

[52]  D. Greig,et al.  The interaction of Saccharomyces paradoxus with its natural competitors on oak bark , 2015, Molecular ecology.

[53]  Sunil Kumar,et al.  Caveats for correlative species distribution modeling , 2015, Ecol. Informatics.

[54]  C. Landry,et al.  Lachancea quebecensis sp. nov., a yeast species consistently isolated from tree bark in the Canadian province of Québec. , 2015, International journal of systematic and evolutionary microbiology.

[55]  C. Kurtzman,et al.  Advances in yeast systematics and phylogeny and their use as predictors of biotechnologically important metabolic pathways. , 2015, FEMS yeast research.

[56]  A. Couloux,et al.  A population genomics insight into the Mediterranean origins of wine yeast domestication , 2015, Molecular ecology.

[57]  G. Liti,et al.  The fascinating and secret wild life of the budding yeast S. cerevisiae , 2015, eLife.

[58]  G. Bell,et al.  Speciation driven by hybridization and chromosomal plasticity in a wild yeast , 2015, Nature Microbiology.