Substrate, temperature, and geographical patterns among nearly 2000 natural yeast isolates

Spurley, William J.; Fisher, Kaitlin J.; Langdon, Quinn K.; Buh, Kelly V.; Jarzyna, Martin; Haase, Max A. B.; Sylvester, Kayla; Moriarty, Ryan V.; Rodriguez, Daniel; Sheddan, Angela; Wright, Sarah; Sorlie, Lisa; Hulfachor, Amanda Beth; Opulente, Dana A.; Hittinger, Chris Todd

doi:10.1002/yea.3679

Title: Substrate, temperature, and geographical patterns among nearly 2000 natural yeast isolates

Journal Article · 04 November 2021 · Yeast

DOI: https://doi.org/10.1002/yea.3679 · OSTI ID:1846256

Spurley, William J. ^[1]; Fisher, Kaitlin J. ^[2]; Langdon, Quinn K. ^[3]; Buh, Kelly V. ^[4]; Jarzyna, Martin ^[4]; Haase, Max A. B. ^[5]; Sylvester, Kayla ^[6]; Moriarty, Ryan V. ^[4]; Rodriguez, Daniel ^[4]; Sheddan, Angela ^[7]; Wright, Sarah ^[8]; Sorlie, Lisa ^[9]; Hulfachor, Amanda Beth ^[4]; Opulente, Dana A. ^[10];

^[4]

Univ. of Wisconsin, Madison, WI (United States); Center for Genomic Science Innovation, University of Wisconsin-Madison
Univ. of Wisconsin, Madison, WI (United States)
Univ. of Wisconsin, Madison, WI (United States); Stanford Univ., CA (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); New York Univ. (NYU), NY (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Duke Univ., Durham, NC (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); West Carroll High School, Savannah, IL (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); EAGLE School of Madison Fitchburg, WI (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); School District of Bonduel, WI (United States)
Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Villanova Univ., PA (United States)

Yeasts have broad importance as industrially and clinically relevant microbes and as powerful models for fundamental research, but we are only beginning to understand the roles yeasts play in natural ecosystems. Yeast ecology is often more difficult to study compared to other, more abundant microbes, but growing collections of natural yeast isolates are beginning to shed light on fundamental ecological questions. In this work, we used environmental sampling and isolation to assemble a dataset of 1962 isolates collected from throughout the contiguous United States of America (USA) and Alaska, which were then used to uncover geographic patterns, along with substrate and temperature associations among yeast taxa. We found some taxa, including the common yeasts Torulaspora delbrueckii and Saccharomyces paradoxus, to be repeatedly isolated from multiple sampled regions of the USA, and we classify these as broadly distributed cosmopolitan yeasts. A number of yeast taxon-substrate associations were identified, some of which were novel and some of which support previously reported associations. Further, we found a strong effect of isolation temperature on the phyla of yeasts recovered, as well as for many species. We speculate that substrate and isolation temperature associations reflect the ecological diversity of and niche partitioning by yeast taxa.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: SC0018409

OSTI ID:: 1846256

Journal Information:: Yeast, Journal Name: Yeast Journal Issue: 1-2 Vol. 39; ISSN 0749-503X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (52)

Impact of Host DNA and Sequencing Depth on the Taxonomic Resolution of Whole Metagenome Sequencing for Microbiome Analysis Pereira-Marques, Joana; Hout, Anne; Ferreira, Rui M. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01277	journal	June 2019
Harnessing yeast metabolism of aromatic amino acids for fermented beverage bioflavouring and bioproduction Cordente, Antonio G.; Schmidt, Simon; Beltran, Gemma Applied Microbiology and Biotechnology, Vol. 103, Issue 11 https://doi.org/10.1007/s00253-019-09840-w	journal	April 2019
Role of social wasps in Saccharomyces cerevisiae ecology and evolution Stefanini, I.; Dapporto, L.; Legras, J. -L. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1208362109	journal	July 2012
Trichosporon porosum comb. nov., an anamorphic basidiomycetous yeast inhabiting soil, related to the loubieri / laibachii group of species that assimilate hemicelluloses and phenolic compounds Middelhoven, Wouter J.; Scorzetti, Gloria; Fell, Jack W. FEMS Yeast Research, Vol. 1, Issue 1 https://doi.org/10.1111/j.1567-1364.2001.tb00009.x	journal	April 2001
Population genomics reveals structure at the individual, host-tree scale and persistence of genotypic variants of the undomesticated yeast Saccharomyces paradoxus in a natural woodland Xia, Wenjing; Nielly-Thibault, Lou; Charron, Guillaume Molecular Ecology, Vol. 26, Issue 4 https://doi.org/10.1111/mec.13954	journal	January 2017
Facts, myths and legends on the prime industrial microorganism Vaughan-Martini, Ann; Martini, Alessandro Journal of Industrial Microbiology, Vol. 14, Issue 6 https://doi.org/10.1007/BF01573967	journal	June 1995
Population genomics shows no distinction between pathogenic Candida krusei and environmental Pichia kudriavzevii: One species, four names Douglass, Alexander P.; Offei, Benjamin; Braun-Galleani, Stephanie PLOS Pathogens, Vol. 14, Issue 7 https://doi.org/10.1371/journal.ppat.1007138	journal	July 2018
Saccharomyces cerevisiae: a nomadic yeast with no niche? Goddard, Matthew R.; Greig, Duncan FEMS Yeast Research, Vol. 15, Issue 3 https://doi.org/10.1093/femsyr/fov009	journal	February 2015
Expansion of the Candida tanzawaensis yeast clade: 16 novel Candida species from basidiocarp-feeding beetles Suh, S. -O. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 6 https://doi.org/10.1099/ijs.0.63246-0	journal	November 2004
Yeasts colonizing the leaves of fruit trees SlÁviková, Elena; Vadkertiová, Renata; Vránová, Dana Annals of Microbiology, Vol. 59, Issue 3 https://doi.org/10.1007/BF03175125	journal	September 2009
Population genomics of domestic and wild yeasts Liti, Gianni; Carter, David M.; Moses, Alan M. Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07743	journal	February 2009
Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America Charron, Guillaume; Leducq, Jean-Baptiste; Bertin, Chloé FEMS Yeast Research, Vol. 14, Issue 2 https://doi.org/10.1111/1567-1364.12100	journal	October 2013
Diverse yeasts for diverse fermented beverages and foods Hittinger, Chris Todd; Steele, James L.; Ryder, David S. Current Opinion in Biotechnology, Vol. 49 https://doi.org/10.1016/j.copbio.2017.10.004	journal	February 2018
Comparative genomics of xylose-fermenting fungi for enhanced biofuel production Wohlbach, D. J.; Kuo, A.; Sato, T. K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 32, p. 13212-13217 https://doi.org/10.1073/pnas.1103039108	journal	July 2011
Intergenic Transcribed Spacer PCR Ribotyping for Differentiation of Saccharomyces Species and Interspecific Hybrids McCullough, Michael J.; Clemons, Karl V.; McCusker, John H. Journal of Clinical Microbiology, Vol. 36, Issue 4 https://doi.org/10.1128/JCM.36.4.1035-1038.1998	journal	January 1998
Toward a Fully Resolved Fungal Tree of Life James, Timothy Y.; Stajich, Jason E.; Hittinger, Chris Todd Annual Review of Microbiology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-micro-022020-051835	journal	July 2020
Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies Chao, Anne; Gotelli, Nicholas J.; Hsieh, T. C. Ecological Monographs, Vol. 84, Issue 1 https://doi.org/10.1890/13-0133.1	journal	February 2014
New pathogens, new tricks: emerging, drug-resistant fungal pathogens and future prospects for antifungal therapeutics: Drug-resistant fungal pathogens Geddes-McAlister, Jennifer; Shapiro, Rebecca S. Annals of the New York Academy of Sciences, Vol. 1435, Issue 1 https://doi.org/10.1111/nyas.13739	journal	May 2018
An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages Nespolo, Roberto F.; Villarroel, Carlos A.; Oporto, Christian I. PLOS Genetics, Vol. 16, Issue 5 https://doi.org/10.1371/journal.pgen.1008777	journal	May 2020
Sequencing and beyond: integrating molecular 'omics' for microbial community profiling Franzosa, Eric A.; Hsu, Tiffany; Sirota-Madi, Alexandra Nature Reviews Microbiology, Vol. 13, Issue 6 https://doi.org/10.1038/nrmicro3451	journal	April 2015
Diverse Lineages of Candida albicans Live on Old Oaks Bensasson, Douda; Dicks, Jo; Ludwig, John M. Genetics, Vol. 211, Issue 1 https://doi.org/10.1534/genetics.118.301482	journal	November 2018
Pathogenic budding yeasts isolated outside of clinical settings Opulente, Dana A.; Langdon, Quinn K.; Buh, Kelly V. FEMS Yeast Research, Vol. 19, Issue 3 https://doi.org/10.1093/femsyr/foz032	journal	April 2019
Yeasts and yeast-like organisms associated with fruits and blossoms of different fruit trees Vadkertiová, Renáta; Molnárová, Jana; Vránová, Dana Canadian Journal of Microbiology, Vol. 58, Issue 12 https://doi.org/10.1139/cjm-2012-0468	journal	December 2012
Local climatic adaptation in a widespread microorganism Leducq, Jean-Baptiste; Charron, Guillaume; Samani, Pedram Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1777 https://doi.org/10.1098/rspb.2013.2472	journal	February 2014
Detection of Delphinella shoot blight in plantations of balsam fir ( Abies balsamea ) Christmas trees in Quebec, Canada Guertin, Julien F.; Zitouni, Mina; Tanguay, Philippe Canadian Journal of Plant Pathology, Vol. 41, Issue 1 https://doi.org/10.1080/07060661.2018.1547791	journal	December 2018
Oleaginous yeast for biofuel and oleochemical production Spagnuolo, Michael; Yaguchi, Allison; Blenner, Mark Current Opinion in Biotechnology, Vol. 57 https://doi.org/10.1016/j.copbio.2019.02.011	journal	June 2019
Isolation and Laboratory Domestication of Natural Yeast Strains Liti, Gianni; Warringer, Jonas; Blomberg, Anders Cold Spring Harbor Protocols, Vol. 2017, Issue 8 https://doi.org/10.1101/pdb.prot089052	journal	August 2017
Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of North American oaks Naumov, Gennadi I.; Naumova, Elena S.; Sniegowski, Paul D. Canadian Journal of Microbiology, Vol. 44, Issue 11 https://doi.org/10.1139/w98-104	journal	November 1998
Associations of Yeasts with Spotted-Wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in Cherries and Raspberries Hamby, Kelly A.; Hernández, Alejandro; Boundy-Mills, Kyria Applied and Environmental Microbiology, Vol. 78, Issue 14 https://doi.org/10.1128/AEM.00841-12	journal	May 2012
Genome evolution across 1,011 Saccharomyces cerevisiae isolates Peter, Jackson; De Chiara, Matteo; Friedrich, Anne Nature, Vol. 556, Issue 7701 https://doi.org/10.1038/s41586-018-0030-5	journal	April 2018
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids Langdon, Quinn K.; Peris, David; Eizaguirre, Juan I. PLOS Genetics, Vol. 16, Issue 4 https://doi.org/10.1371/journal.pgen.1008680	journal	April 2020
Genetic identification of biological species in theSaccharomyces sensu stricto complex Naumov, Gl Journal of Industrial Microbiology & Biotechnology, Vol. 17, Issue 3-4 https://doi.org/10.1007/BF01574704	journal	September 1996
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5471	journal	July 2014
Quantifying the individual effects of ethanol and temperature on the fitness advantage of Saccharomyces cerevisiae Salvadó, Z.; Arroyo-López, F. N.; Barrio, E. Food Microbiology, Vol. 28, Issue 6 https://doi.org/10.1016/j.fm.2011.03.008	journal	September 2011
Quest for wine yeasts—An old story revisited Török, T.; Mortimer, Rk; Romano, P. Journal of Industrial Microbiology & Biotechnology, Vol. 17, Issue 3-4 https://doi.org/10.1007/BF01574705	journal	September 1996
Characteristics of a disease of Sphagnum fuscum caused by Scleroconidioma sphagnicola Tsuneda, A.; Chen, M. H.; Currah, R. S. Canadian Journal of Botany, Vol. 79, Issue 10 https://doi.org/10.1139/b01-102	journal	October 2001
Quantifying separation and similarity in a Saccharomyces cerevisiae metapopulation Knight, Sarah; Goddard, Matthew R. The ISME Journal, Vol. 9, Issue 2 https://doi.org/10.1038/ismej.2014.132	journal	July 2014
The Antarctic yeast Candida sake: Understanding cold metabolism impact on wine Ballester-Tomás, Lidia; Prieto, Jose A.; Gil, Jose V. International Journal of Food Microbiology, Vol. 245 https://doi.org/10.1016/j.ijfoodmicro.2017.01.009	journal	March 2017
Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species Sylvester, Kayla; Wang, Qi-Ming; James, Brielle FEMS Yeast Research, Vol. 15, Issue 3 https://doi.org/10.1093/femsyr/fov002	journal	March 2015
Isolation and Identification of Yeasts from Wild Flowers Collected around Jangseong Lake in Jeollanam-do, Republic of Korea, and Characterization of the Unrecorded Yeast Bullera coprosmaensis Han, Sang-Min; Hyun, Se-Hee; Lee, Hyang Burm Mycobiology, Vol. 43, Issue 3 https://doi.org/10.5941/MYCO.2015.43.3.266	journal	September 2015
Functional and evolutionary characterization of a secondary metabolite gene cluster in budding yeasts Krause, David J.; Kominek, Jacek; Opulente, Dana A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 43 https://doi.org/10.1073/pnas.1806268115	journal	October 2018
Curvibasidium cygneicollum gen. nov., sp. nov. and Curvibasidium pallidicorallinum sp. nov., novel taxa in the Microbotryomycetidae (Urediniomycetes), and their relationship with Rhodotorula fujisanensis and Rhodotorula nothofagi Sampaio, José Paulo; Golubev, Wladyslav I.; Fell, Jack W. International Journal of Systematic and Evolutionary Microbiology, Vol. 54, Issue 4 https://doi.org/10.1099/ijs.0.03037-0	journal	July 2004
Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics Sniegowski, Paul D.; Dombrowski, Peter G.; Fingerman, Ethan FEMS Yeast Research, Vol. 1, Issue 4 https://doi.org/10.1111/j.1567-1364.2002.tb00048.x	journal	January 2002
Quantifying the efficiency and biases of forest Saccharomyces sampling strategies Boynton, Primrose J.; Kowallik, Vienna; Landermann, Doreen Yeast, Vol. 36, Issue 11 https://doi.org/10.1002/yea.3435	journal	August 2019
Occurrence and Distribution of Fungi in a Subtropical Marine Environment Roth Jr., F. J.; Orpurt, P. A.; Ahearn, D. G. Canadian Journal of Botany, Vol. 42, Issue 4 https://doi.org/10.1139/b64-037	journal	April 1964
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus Peris, David; Langdon, Quinn K.; Moriarty, Ryan V. PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006155	journal	July 2016
Sydowia polyspora associated with current season needle necrosis (CSNN) on true fir (Abies spp.) Talgø, Venche; Chastagner, Gary; Thomsen, Iben Margrete Fungal Biology, Vol. 114, Issue 7 https://doi.org/10.1016/j.funbio.2010.04.005	journal	July 2010
High-throughput sequencing view on the magnitude of global fungal diversity Baldrian, Petr; Větrovský, Tomáš; Lepinay, Clémentine Fungal Diversity https://doi.org/10.1007/s13225-021-00472-y	journal	February 2021
Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids: New Zealand Saccharomyces ecology Zhang, Hanyao; Skelton, Aaron; Gardner, Richard C. FEMS Yeast Research, Vol. 10, Issue 7 https://doi.org/10.1111/j.1567-1364.2010.00681.x	journal	September 2010
Summer temperature can predict the distribution of wild yeast populations Robinson, Heather A.; Pinharanda, Ana; Bensasson, Douda Ecology and Evolution, Vol. 6, Issue 4 https://doi.org/10.1002/ece3.1919	journal	January 2016
A systematic forest survey showing an association of Saccharomyces paradoxus with oak leaf litter Kowallik, Vienna; Greig, Duncan Environmental Microbiology Reports, Vol. 8, Issue 5 https://doi.org/10.1111/1758-2229.12446	journal	August 2016
Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity Wang, Qi-Ming; Liu, Wan-Qiu; Liti, Gianni Molecular Ecology, Vol. 21, Issue 22 https://doi.org/10.1111/j.1365-294X.2012.05732.x	journal	August 2012

Similar Records

Oxygen requirements of yeasts. [Saccharomyces cerevisiae; Candida tropicalis]

Journal Article · 1990 · Applied and Environmental Microbiology; (USA) · OSTI ID:5962398

Visser, W; Scheffers, W A; Batenburg-Van Der Vegte, W H; +1 more

Induction and characterization of artificial diploids from the haploid yeast Torulaspora delbrueckii

Journal Article · 1987 · Appl. Environ. Microbiol.; (United States) · OSTI ID:5934495

Sasaki, T; Ohshima, Y

Early fermentation volatile metabolite profile of non-Saccharomyces yeasts in red and white grape must: A targeted approach

Journal Article · 2015 · Lebensmittel-Wissenschaft + Technologie · OSTI ID:1339389

Beckner Whitener, Margaret E.; Carlin, Silvia; Jacobson, Dan; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Ascomycota
Basidiomycota
Saccharomyces
ecology
fungi
yeasts.

Title: Substrate, temperature, and geographical patterns among nearly 2000 natural yeast isolates

Citation Formats

References (52)

Linked Research (1)

Similar Records

Related Subjects