Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids
Autoři:
Quinn K. Langdon aff001; David Peris aff001; Juan I. Eizaguirre aff004; Dana A. Opulente aff001; Kelly V. Buh aff001; Kayla Sylvester aff001; Martin Jarzyna aff001; María E. Rodríguez aff005; Christian A. Lopes aff005; Diego Libkind aff004; Chris Todd Hittinger aff001
Působiště autorů:
Laboratory of Genetics, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy Institute, Center for Genomic Science Innovation, University of Wisconsin-Madison, Madison, United States of America
aff001; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States of America
aff002; Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA), CSIC, Valencia, Spain
aff003; Centro de Referencia en Levaduras y Tecnología Cervecera (CRELTEC), Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC) – CONICET / Universidad Nacional del Comahue, Quintral 1250, Bariloche, Argentina
aff004; Laboratorio de Microbiología Aplicada, Biotecnología y Bioinformática de Levaduras, Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Consejo Nacional de Investigaciones, Científicas y Técnicas (CONICET)-Universidad Nacional
aff004; Instituto de Investigación y Desarrollo en Ingeniería de Procesos, Biotecnología y Energías Alternativas (PROBIEN, CONICET-UNCo), Neuquén, Argentina
aff005
Vyšlo v časopise:
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008680
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008680
Souhrn
The wild, cold-adapted parent of hybrid lager-brewing yeasts, Saccharomyces eubayanus, has a complex and understudied natural history. The exploration of this diversity can be used both to develop new brewing applications and to enlighten our understanding of the dynamics of yeast evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. eubayanus strains, the largest collection known to date. S. eubayanus has a multilayered population structure, consisting of two major populations that are further structured into six subpopulations. Four of these subpopulations are found exclusively in the Patagonian region of South America; one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is specific to the Holarctic ecozone. Plant host associations differed between subpopulations and between S. eubayanus and its sister species, Saccharomyces uvarum. S. eubayanus is most abundant and genetically diverse in northern Patagonia, where some locations harbor more genetic diversity than is found outside of South America, suggesting that northern Patagonia east of the Andes was a glacial refugium for this species. All but one subpopulation shows isolation-by-distance, and gene flow between subpopulations is low. However, there are strong signals of ancient and recent outcrossing, including two admixed lineages, one that is sympatric with and one that is mostly isolated from its parental populations. Using our extensive biogeographical data, we build a robust model that predicts all known and a handful of additional regions of the globe that are climatically suitable for S. eubayanus, including Europe where host accessibility and competitive exclusion by other Saccharomyces species may explain its continued elusiveness. We conclude that this industrially relevant species has rich natural diversity with many factors contributing to its complex distribution and natural history.
Klíčová slova:
Biogeography – Europe – Nucleotide sequencing – Phylogeography – Saccharomyces – Saccharomyces cerevisiae – South America – Species diversity
Zdroje
1. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, et al. Population genomics of domestic and wild yeasts. Nature. 2009;458: 337–341. doi: 10.1038/nature07743 19212322
2. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature. 2009;458: 342–5. doi: 10.1038/nature07670 19212320
3. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, et al. Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts. Cell. 2016;166: 1397–1410.e16. doi: 10.1016/j.cell.2016.08.020 27610566
4. Gonçalves M, Pontes A, Almeida P, Barbosa R, Serra M, Libkind D, et al. Distinct Domestication Trajectories in Top- Fermenting Beer Yeasts and Wine Yeasts. Curr Biol. 2016;26: 1–12. doi: 10.1016/j.cub.2015.11.020
5. Leducq J-B, Charron G, Samani P, Dubé AK, Sylvester K, James B, et al. Local climatic adaptation in a widespread microorganism. Proc Biol Sci. 2014;281: 20132472. doi: 10.1098/rspb.2013.2472 24403328
6. Eberlein C, Hénault M, Fijarczyk A, Charron G, Bouvier M, Kohn LM, et al. Hybridization is a recurrent evolutionary stimulus in wild yeast speciation. Nat Commun. 2019;10. doi: 10.1038/s41467-019-08809-7 30804385
7. Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J, Johnston M, et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A. 2011;108: 14539–44. doi: 10.1073/pnas.1105430108 21873232
8. Gibson B, Liti G. Saccharomyces pastorianus: genomic insights inspiring innovation for industry. Yeast. 2015;32: 17–27. doi: 10.1002/yea.3033 25088523
9. Hittinger CT, Steele JL, Ryder DS. Diverse yeasts for diverse fermented beverages and foods. Curr Opin Biotechnol. 2018;49: 199–206. doi: 10.1016/j.copbio.2017.10.004 29102814
10. Baker EP, Peris D, Moriarty R V, Li XC, Fay JC, Hittinger CT. Mitochondrial DNA and temperature tolerance in lager yeasts. Sci Adv. 2019;5: eaav1869. doi: 10.1126/sciadv.aav1869 30729163
11. Almeida P, Gonçalves C, Teixeira S, Libkind D, Bontrager M, Masneuf-Pomarède I, et al. A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat Commun. 2014;5: 4044. doi: 10.1038/ncomms5044 24887054
12. Nguyen HV, Boekhout T. Characterization of Saccharomyces uvarum (Beijerinck, 1898) and related hybrids: Assessment of molecular markers that predict the parent and hybrid genomes and a proposal to name yeast hybrids. FEMS Yeast Res. 2017;17: 1–19. doi: 10.1093/femsyr/fox014 28334169
13. Langdon QK, Peris D, Baker EP, Opulente DA, Nguyen H-V, Bond U, et al. Fermentation innovation through complex hybridization of wild and domesticated yeasts. Nat Ecol Evol. 2019. doi: 10.1038/s41559-019-0998-8 31636426
14. Gallone B, Steensels J, Mertens S, Dzialo MC, Gordon JL, Wauters R, et al. Interspecific hybridization facilitates niche adaptation in beer yeast. Nat Ecol Evol. 2019;3: 1562–1575. doi: 10.1038/s41559-019-0997-9 31636425
15. Sampaio JP. Microbe profile: Saccharomyces eubayanus, the missing link to lager beer yeasts. Microbiol (United Kingdom). 2018;164: 1069–1071. doi: 10.1099/mic.0.000677 30175956
16. Bing J, Han P-J, Liu W-Q, Wang Q-M, Bai F-Y. Evidence for a Far East Asian origin of lager beer yeast. Curr Biol. 2014;24: R380–1. doi: 10.1016/j.cub.2014.04.031 24845661
17. Peris D, Sylvester K, Libkind D, Gonçalves P, Sampaio JP, Alexander WG, et al. Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol. 2014;23: 2031–2045. doi: 10.1111/mec.12702 24612382
18. Rodríguez ME, Pérez-Través L, Sangorrín MP, Barrio E, Lopes CA. Saccharomyces eubayanus and Saccharomyces uvarum associated with the fermentation of Araucaria araucana seeds in Patagonia. FEMS Yeast Res. 2014;14: 948–965. doi: 10.1111/1567-1364.12183 25041507
19. Gayevskiy V, Goddard MR. Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests. Environ Microbiol. 2016;18: 1137–1147. doi: 10.1111/1462-2920.13107 26522264
20. Peris D, Langdon QK, Moriarty R V, Sylvester K, Bontrager M, Charron G, et al. Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus. PLoS Genet. 2016;12. doi: 10.1371/journal.pgen.1006155 27385107
21. Eizaguirre JI, Peris D, Rodríguez ME, Lopes CA, De Los Ríos P, Hittinger CT, et al. Phylogeography of the wild Lager-brewing ancestor (Saccharomyces eubayanus) in Patagonia. Environ Microbiol. 2018;20: 3732–3743. doi: 10.1111/1462-2920.14375 30105823
22. Sampaio JP, Gonçalves P. Biogeography and Ecology of the Genus Saccharomyces. Yeasts in Natural Ecosystems: Ecology. 2017. pp. 131–157.
23. Naseeb S, Alsammar H, Burgis T, Donaldson I, Knyazev N, Knight C, et al. Whole Genome Sequencing, de Novo Assembly and Phenotypic Profiling for the New Budding Yeast Species Saccharomyces jurei. G3. 2018;8: 2967–2977. doi: 10.1534/g3.118.200476 30097472
24. Wang Q-M, Liu W-Q, Liti G, Wang S-A, Bai F-Y. Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol Ecol. 2012;21: 5404–5417. doi: 10.1111/j.1365-294X.2012.05732.x 22913817
25. Boynton PJ, Greig D. The ecology and evolution of non-domesticated Saccharomyces species. Yeast. 2014;31: 449–462. doi: 10.1002/yea.3040 25242436
26. Robinson HA, Pinharanda A, Bensasson D. Summer temperature can predict the distribution of wild yeast populations. Ecol Evol. 2016;6: 1236–1250. doi: 10.1002/ece3.1919 26941949
27. Brouwers N, Brickwedde A, Gorter de Vries AR, van den Broek M, Weening SM, van den Eijnden L, et al. Maltotriose consumption by hybrid Saccharomyces pastorianus is heterotic and results from regulatory cross-talk between parental sub-genomes. bioRxiv. 2019; 679563. doi: 10.1101/679563
28. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24: 1403–1405. doi: 10.1093/bioinformatics/btn129 18397895
29. Huson DH, Bryant D. Application of Phylogenetic Networks in Evolutionary Studies. Mol Biol Evol. 2006;23: 254–267. doi: 10.1093/molbev/msj030 16221896
30. Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet. 2012;8: e1002453. doi: 10.1371/journal.pgen.1002453 22291602
31. Raj A, Stephens M, Pritchard JK. fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets. Genetics. 2014;197: 573–589. doi: 10.1534/genetics.114.164350 24700103
32. Leducq J-B, Nielly-Thibault L, Charron G, Eberlein C, Verta J-P, Samani P, et al. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat Microbiol. 2016;1: 1–10. doi: 10.1038/nmicrobiol.2015.3 27571751
33. Salema-Oom M, Pinto VV, Gonçalves P, Spencer-Martins I. Maltotriose Utilization by Industrial. Society. 2005;71: 5044–5049. doi: 10.1128/AEM.71.9.5044
34. Gibson BR, Storgårds E, Krogerus K, Vidgren V. Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus. Yeast. 2013;30: 255–266. doi: 10.1002/yea.2960 23695993
35. Hittinger CT. Saccharomyces diversity and evolution: a budding model genus. Trends Genet. 2013;29: 309–17. doi: 10.1016/j.tig.2013.01.002 23395329
36. Peter J, De Chiara M, Friedrich A, Yue JX, Pflieger D, Bergström A, et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature. 2018;556: 339–344. doi: 10.1038/s41586-018-0030-5 29643504
37. Mathiasen P, Premoli AC. Out in the cold: Genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America. Mol Ecol. 2010;19: 371–385. doi: 10.1111/j.1365-294X.2009.04456.x 20002584
38. Premoli AC, Mathiasen P, Kitzberger T. Southern-most Nothofagus trees enduring ice ages: Genetic evidence and ecological niche retrodiction reveal high latitude (54°S) glacial refugia. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;298: 247–256. doi: 10.1016/J.PALAEO.2010.09.030
39. Quiroga MP, Premoli AC. Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;285: 186–193. doi: 10.1016/J.PALAEO.2009.11.010
40. Kass JM, Vilela B, Aiello-Lammens ME, Muscarella R, Merow C, Anderson RP. Wallace: A flexible platform for reproducible modeling of species niches and distributions built for community expansion. O’Hara RB, editor. Methods Ecol Evol. 2018;9: 1151–1156. doi: 10.1111/2041-210X.12945
41. Nespolo RF, Villarroel CA, Oporto CI, Tapia SM, Vega F, Urbina K, et al. An Out-of-Patagonia dispersal explains most of the worldwide genetic distribution in Saccharomyces eubayanus. Submiss. 2019. https://www.biorxiv.org/content/10.1101/709253v1
42. Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK. Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol. 2012;27: 47–56. doi: 10.1016/j.tree.2011.08.009 22014977
43. Francesca N, Canale DE, Settanni L, Moschetti G. Dissemination of wine-related yeasts by migratory birds. Environ Microbiol Rep. 2012;4: 105–112. doi: 10.1111/j.1758-2229.2011.00310.x 23757236
44. Francesca N, Carvalho C, Sannino C, Guerreiro M a, Almeida PM, Settanni L, et al. Yeasts vectored by migratory birds collected in the Mediterranean island of Ustica and description of Phaffomyces usticensis f.a. sp. nov., a new species related to the cactus ecoclade. FEMS Yeast Res. 2014;14: 910–21. doi: 10.1111/1567-1364.12179 24981278
45. Stefanini I, Dapporto L, Legras J-L, Calabretta A, Di Paola M, De Filippo C, et al. Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc Natl Acad Sci U S A. 2012;109: 13398–403. doi: 10.1073/pnas.1208362109 22847440
46. Kuehne HA, Murphy HA, Francis CA, Sniegowski PD. Allopatric Divergence, Secondary Contact, and Genetic Isolation in Wild Yeast Populations. Curr Biol. 2007;17: 407–411. doi: 10.1016/j.cub.2006.12.047 17306538
47. Stewart JR, Lister AM. Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol. 2001;16: 608–613. doi: 10.1016/S0169-5347(01)02338-2
48. Premoli AC, Mathiasen P, Cristina Acosta M, Ramos VA. Phylogeographically concordant chloroplast DNA divergence in sympatric Nothofagus s.s. How deep can it be? New Phytol. 2012;193: 261–275. doi: 10.1111/j.1469-8137.2011.03861.x 21883239
49. Alsammar HF, Naseeb S, Brancia LB, Gilman RT, Wang P, Delneri D. Targeted metagenomics approach to capture the biodiversity of Saccharomyces genus in wild environments. Environ Microbiol Rep. 2019;11: 206–214. doi: 10.1111/1758-2229.12724 30507071
50. Czekanski-Moir JE, Rundell RJ. The Ecology of Nonecological Speciation and Nonadaptive Radiations. Trends Ecol Evol. 2019;34: 400–415. doi: 10.1016/j.tree.2019.01.012 30824193
51. Pool JE, Corbett-Detig RB, Sugino RP, Stevens K a, Cardeno CM, Crepeau MW, et al. Population Genomics of sub-saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet. 2012;8: e1003080. doi: 10.1371/journal.pgen.1003080 23284287
52. Nielsen R, Akey JM, Jakobsson M, Pritchard JK, Tishkoff S, Willerslev E. Tracing the peopling of the world through genomics. Nature. 2017;541: 302–310. doi: 10.1038/nature21347 28102248
53. Racimo F, Sankararaman S, Nielsen R, Huerta-Sánchez E. Evidence for archaic adaptive introgression in humans. Nat Rev Genet. 2015;16: 359–371. doi: 10.1038/nrg3936 25963373
54. Marsit S, Leducq JB, Durand É, Marchant A, Filteau M, Landry CR. Evolutionary biology through the lens of budding yeast comparative genomics. Nat Rev Genet. 2017;18: 581–598. doi: 10.1038/nrg.2017.49 28714481
55. Yurkov A. Temporal and Geographic Patterns in Yeast Distribution. Yeasts in Natural Ecosystems: Ecology. 2017. pp. 101–130.
56. Baas-Becking L. Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NV; 1934.
57. de Wit R, Bouvier T. “Everything is everywhere, but, the environment selects”; what did Baas Becking and Beijerinck really say? Environ Microbiol. 2006;8: 755–758. doi: 10.1111/j.1462-2920.2006.01017.x 16584487
58. Sylvester K, Wang Q-M, James B, Mendez R, Hulfachor AB, Hittinger CT. Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species. FEMS Yeast Res. 2015;15: fov002. doi: 10.1093/femsyr/fov002 25743785
59. Shen X-X, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh K V., et al. Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum. Cell. 2018;175: 1533–1545.e20. doi: 10.1016/j.cell.2018.10.023 30415838
60. Baker E, Wang B, Bellora N, Peris D, Hulfachor AB, Koshalek JA, et al. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol Biol Evol. 2015;32: 2818–2831. doi: 10.1093/molbev/msv168 26269586
61. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. doi: 10.1101/gr.107524.110 20644199
62. Pfeifer B, Wittelsbuerger U. Package ‘PopGenome.’ 2015. doi: 10.1111/rssb.12200
63. Zhang C, Dong S-S, Xu J-Y, He W-M, Yang T-L. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019;35: 1786–1788. doi: 10.1093/bioinformatics/bty875 30321304
64. Hijmans RJ, Williams E, Vennes C. Package “geosphere” Type Package Title Spherical Trigonometry. 2019.
65. Dray S, Dufour A-B. The ade4 Package: Implementing the Duality Diagram for Ecologists. J Stat Softw. 2007;22: 1–20. doi: 10.18637/jss.v022.i04
66. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal. 2006;1695: 1–9.
67. Kahm M, Hasenbrink G, Lichtenberg-Fraté H, Ludwig J, Kschischo M. grofit: Fitting Biological Growth Curves with R. J Stat Softw. 2010;33: 1–21. doi: 10.18637/jss.v033.i07
68. Suzuki R, Shimodaira H. Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22: 1540–1542. doi: 10.1093/bioinformatics/btl117 16595560
69. Lamprecht MR, Sabatini DM, Carpenter AE. CellProfilerTM: Free, versatile software for automated biological image analysis. Biotechniques. 2007;42: 71–75. doi: 10.2144/000112257 17269487
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