An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages
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Roberto F. Nespolo aff001; Carlos A. Villarroel aff002; Christian I. Oporto aff002; Sebastián M. Tapia aff002; Franco Vega-Macaya aff002; Kamila Urbina aff002; Matteo De Chiara aff005; Simone Mozzachiodi aff005; Ekaterina Mikhalev aff006; Dawn Thompson aff006; Luis F. Larrondo aff002; Pablo Saenz-Agudelo aff001; Gianni Liti aff005; Francisco A. Cubillos aff002
Působiště autorů:
Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile
aff001; Millennium Institute for Integrative Biology (iBio), Santiago, Chile
aff002; Center of Applied Ecology and Sustainability (CAPES), Santiago, Chile
aff003; Universidad de Santiago de Chile, Facultad de Química y Biología, Departamento de Biología, Santiago, Chile
aff004; Université Côte d’Azur, CNRS, INSERM, IRCAN, Nice, France
aff005; Ginkgo Bioworks, Boston, Massachusetts, United States of America
aff006; Departamento Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
aff007
Vyšlo v časopise:
An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008777
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008777
Souhrn
Population‐level sampling and whole‐genome sequences of different individuals allow one to identify signatures of hybridization, gene flow and potential molecular mechanisms of environmental responses. Here, we report the isolation of 160 Saccharomyces eubayanus strains, the cryotolerant ancestor of lager yeast, from ten sampling sites in Patagonia along 2,000 km of Nothofagus forests. Frequency of S. eubayanus isolates was higher towards southern and colder regions, demonstrating the cryotolerant nature of the species. We sequenced the genome of 82 strains and, together with 23 available genomes, performed a comprehensive phylogenetic analysis. Our results revealed the presence of five different lineages together with dozens of admixed strains. Various analytical methods reveal evidence of gene flow and historical admixture between lineages from Patagonia and Holarctic regions, suggesting the co-occurrence of these ancestral populations. Analysis of the genetic contribution to the admixed genomes revealed a Patagonian genetic origin of the admixed strains, even for those located in the North Hemisphere. Overall, the Patagonian lineages, particularly the southern populations, showed a greater global genetic diversity compared to Holarctic and Chinese lineages, in agreement with a higher abundance in Patagonia. Thus, our results are consistent with a likely colonization of the species from peripheral glacial refugia from South Patagonia. Furthermore, fermentative capacity and maltose consumption resulted negatively correlated with latitude, indicating better fermentative performance in northern populations. Our genome analysis, together with previous reports in the sister species S. uvarum suggests that a S. eubayanus ancestor was adapted to the harsh environmental conditions of Patagonia, a region that provides the ecological conditions for the diversification of these ancestral lineages.
Klíčová slova:
Fermentation – Chile (country) – Phylogenetic analysis – Phylogeography – Population genetics – Saccharomyces – Saccharomyces cerevisiae – Species diversity
Zdroje
1. Arnold ML. Evolution Through Genetic Exchange. Evolution through Genetic Exchange. 2007:1–252. doi: 10.1093/acprof:oso/9780199229031.001.0001
2. Gladieux P, Wilson BA, Perraudeau F, Montoya LA, Kowbel D, Hann-Soden C, et al. Genomic sequencing reveals historical, demographic and selective factors associated with the diversification of the fire-associated fungus Neurospora discreta. Mol Ecol. 2015;24(22):5657–75. Epub 2015/10/11. doi: 10.1111/mec.13417. 26453896.
3. Dujon BA, Louis EJ. Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina). Genetics. 2017;206(2):717–50. doi: 10.1534/genetics.116.199216. 28592505.
4. Borneman AR, Pretorius IS. Genomic insights into the Saccharomyces sensu stricto complex. Genetics. 2015;199(2):281–91. doi: 10.1534/genetics.114.173633. 25657346; PubMed Central PMCID: PMC4317643.
5. Peter J, De Chiara M, Friedrich A, Yue JX, Pflieger D, Bergstrom A, et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature. 2018;556(7701):339–44. doi: 10.1038/s41586-018-0030-5. 29643504.
6. Legras JL, Galeote V, Bigey F, Camarasa C, Marsit S, Nidelet T, et al. Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication. Mol Biol Evol. 2018;35(7):1712–27. doi: 10.1093/molbev/msy066. 29746697; PubMed Central PMCID: PMC5995190.
7. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, et al. Population genomics of domestic and wild yeasts. Nature. 2009;458(7236):337–41. Epub 2009/02/13. doi: 10.1038/nature07743. 19212322; PubMed Central PMCID: PMC2659681.
8. 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(6):1397–410 e16. doi: 10.1016/j.cell.2016.08.020. 27610566; PubMed Central PMCID: PMC5018251.
9. Goncalves 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(20):2750–61. doi: 10.1016/j.cub.2016.08.040. 27720622.
10. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature. 2009;458(7236):342–5. doi: 10.1038/nature07670. 19212320; PubMed Central PMCID: PMC2782482.
11. Yue JX, Li J, Aigrain L, Hallin J, Persson K, Oliver K, et al. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat Genet. 2017. doi: 10.1038/ng.3847. 28416820.
12. Boynton PJ, Greig D. The ecology and evolution of non-domesticated Saccharomyces species. Yeast. 2014;31(12):449–62. doi: 10.1002/yea.3040 25242436
13. Almeida P, Goncalves C, Teixeira S, Libkind D, Bontrager M, Masneuf-Pomarede 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.
14. Eberlein C, Henault 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(1):923. Epub 2019/02/26. doi: 10.1038/s41467-019-08809-7. 30804385; PubMed Central PMCID: PMC6389940.
15. Tilakaratna V, Bensasson D. Habitat Predicts Levels of Genetic Admixture in Saccharomyces cerevisiae. G3 (Bethesda, Md). 2017;7(9):2919–29. doi: 10.1534/g3.117.041806. 28696926.
16. Goddard MR, Greig D. Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res. 2015;15(3). Epub 2015/03/01. doi: 10.1093/femsyr/fov009. 25725024; PubMed Central PMCID: PMC4444983.
17. Krogerus K, Magalhaes F, Vidgren V, Gibson B. Novel brewing yeast hybrids: creation and application. Appl Microbiol Biotechnol. 2017;101(1):65–78. doi: 10.1007/s00253-016-8007-5. 27885413; PubMed Central PMCID: PMC5203825.
18. 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(11):2818–31. doi: 10.1093/molbev/msv168. 26269586; PubMed Central PMCID: PMC4651232.
19. Libkind D, Hittinger CT, Valerio E, Goncalves 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(35):14539–44. doi: 10.1073/pnas.1105430108. 21873232; PubMed Central PMCID: PMC3167505.
20. Eizaguirre JI, Peris D, Rodriguez ME, Lopes CA, De Los Rios P, Hittinger CT, et al. Phylogeography of the wild Lager-brewing ancestor (Saccharomyces eubayanus) in Patagonia. Environ Microbiol. 2018. doi: 10.1111/1462-2920.14375. 30105823.
21. Gayevskiy V, Goddard MR. Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests. Environ Microbiol. 2016;18(4):1137–47. doi: 10.1111/1462-2920.13107. 26522264.
22. Peris D, Sylvester K, Libkind D, Goncalves P, Sampaio JP, Alexander WG, et al. Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol. 2014;23(8):2031–45. doi: 10.1111/mec.12702. 24612382.
23. Langdon QK, Peris D, Eizaguirre JI, Opulente DA, Buh KV, Sylvester K, et al. Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids. PLoS Genet. 2020;16(4):e1008680. doi: 10.1371/journal.pgen.1008680. 32251477.
24. Bing J, Han PJ, Liu WQ, Wang QM, Bai FY. Evidence for a Far East Asian origin of lager beer yeast. Curr Biol. 2014;24(10):R380–1. doi: 10.1016/j.cub.2014.04.031. 24845661.
25. Peris D, Langdon QK, Moriarty RV, 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(7):e1006155. doi: 10.1371/journal.pgen.1006155. 27385107; PubMed Central PMCID: PMC4934787.
26. Cubillos FA, Gibson B, Grijalva-Vallejos N, Krogerus K, Nikulin J. Bioprospecting for brewers: Exploiting natural diversity for naturally diverse beers. Yeast. 2019. doi: 10.1002/yea.3380. 30698853.
27. Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci U S A. 2009;106(38):16333–8. doi: 10.1073/pnas.0904673106. 19805302; PubMed Central PMCID: PMC2740733.
28. Hinojosa LF, Gaxiola A, Pérez MF, Carvajal F, Campano MF, Quattrocchio M, et al. Non-congruent fossil and phylogenetic evidence on the evolution of climatic niche in the Gondwana genus Nothofagus. Journal of Biogeography. 2016;43(3):555–67. doi: 10.1111/jbi.12650
29. de Porras ME, Maldonado A, Abarzua AM, Cardenas ML, Francois JP, Martel-Cea A, et al. Postglacial vegetation, fire and climate dynamics at Central Chilean Patagonia (Lake Shaman, 44 degrees S). Quaternary Sci Rev. 2012;50:71–85. doi: 10.1016/j.quascirev.2012.06.015. WOS:000309434000006.
30. Ponce JF, Fernández M. Climatic and Environmental History of Isla de los Estados, Argentina: Springer Netherlands; 2014.
31. Hildebrand-Vogel R, Godoy R, Vogel A. Subantarctic-Andean Nothofagus pumilio Forests: Distribution Area and Synsystematic Overview; Vegetation and Soils as Demonstrated by an Example of a South Chilean Stand. Vegetatio. 1990;89(1):55–68.
32. Hill RS. Nothofagus: Evolution from a southern perspective. Trends Ecol Evol. 1992;7(6):190–4. doi: 10.1016/0169-5347(92)90071-I. 21236005.
33. Duan S-F, Han P-J, Wang Q-M, Liu W-Q, Shi J-Y, Li K, et al. The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nature Communications. 2018;9(1):2690. doi: 10.1038/s41467-018-05106-7 30002370
34. SÉRsic AN, Cosacov A, Cocucci AA, Johnson LA, Pozner R, Avila LJ, et al. Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biological Journal of the Linnean Society. 2011;103(2):475–94. doi: 10.1111/j.1095-8312.2011.01656.x
35. Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecol Lett. 2004;7(12):1225–41. doi: 10.1111/j.1461-0248.2004.00684.x
36. Sampaio JP, Goncalves P. Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol. 2008;74(7):2144–52. doi: 10.1128/AEM.02396-07. 18281431; PubMed Central PMCID: PMC2292605.
37. J White T, Bruns T, Lee S, Taylor J, A Innis M, H Gelfand D, et al. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. 311990. p. 315–22.
38. Brickwedde A, Brouwers N, van den Broek M, Gallego Murillo JS, Fraiture JL, Pronk JT, et al. Structural, Physiological and Regulatory Analysis of Maltose Transporter Genes in Saccharomyces eubayanus CBS 12357(T). Front Microbiol. 2018;9:1786. doi: 10.3389/fmicb.2018.01786. 30147677; PubMed Central PMCID: PMC6097016.
39. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–i90. Epub 2018/11/14. doi: 10.1093/bioinformatics/bty560. 30423086; PubMed Central PMCID: PMC6129281.
40. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM2013.
41. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43(5):491–8. Epub 2011/04/12. doi: 10.1038/ng.806. 21478889; PubMed Central PMCID: PMC3083463.
42. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012;6(2):80–92. Epub 2012/06/26. doi: 10.4161/fly.19695. 22728672; PubMed Central PMCID: PMC3679285.
43. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. Epub 2014/11/06. doi: 10.1093/molbev/msu300. 25371430; PubMed Central PMCID: PMC4271533.
44. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol Biol Evol. 2018;35(2):518–22. Epub 2017/10/28. doi: 10.1093/molbev/msx281. 29077904; PubMed Central PMCID: PMC5850222.
45. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. Epub 2011/06/10. doi: 10.1093/bioinformatics/btr330. 21653522; PubMed Central PMCID: PMC3137218.
46. Li YL, Liu JX. StructureSelector: A web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour. 2018;18(1):176–7. Epub 2017/09/19. doi: 10.1111/1755-0998.12719. 28921901.
47. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–20. Epub 2005/06/23. doi: 10.1111/j.1365-294X.2005.02553.x. 15969739.
48. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15(5):1179–91. Epub 2015/02/17. doi: 10.1111/1755-0998.12387. 25684545; PubMed Central PMCID: PMC4534335.
49. Ramasamy RK, Ramasamy S, Bindroo BB, Naik VG. STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface. SpringerPlus. 2014;3(1):431. doi: 10.1186/2193-1801-3-431 25152854
50. Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS genetics. 2006;2(12):e190–e. doi: 10.1371/journal.pgen.0020190. 17194218.
51. Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of Population Structure using Dense Haplotype Data. PLOS Genetics. 2012;8(1):e1002453. doi: 10.1371/journal.pgen.1002453 22291602
52. Browning SR, Browning BL. Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies By Use of Localized Haplotype Clustering. The American Journal of Human Genetics. 2007;81(5):1084–97. doi: 10.1086/521987 17924348
53. Cubillos FA, Billi E, Zorgo E, Parts L, Fargier P, Omholt S, et al. Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol. 2011. Epub 2011/01/26. doi: 10.1111/j.1365-294X.2011.05005.x. 21261765.
54. Pickrell JK, Pritchard JK. Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data. PLOS Genetics. 2012;8(11):e1002967. doi: 10.1371/journal.pgen.1002967 23166502
55. Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N, Zhan Y, et al. Ancient Admixture in Human History. Genetics. 2012;192(3):1065–93. doi: 10.1534/genetics.112.145037 22960212
56. Milanesi M, Capomaccio S, Vajana E, Bomba L, Garcia JF, Ajmone-Marsan P, et al. BITE: an R package for biodiversity analyses. bioRxiv. 2017:181610. doi: 10.1101/181610
57. Petr M, Vernot B, Kelso J. admixr—R package for reproducible analyses using ADMIXTOOLS. Bioinformatics. 2019;35(17):3194–5. doi: 10.1093/bioinformatics/btz030 30668635
58. Leppälä K, Nielsen SV, Mailund T. admixturegraph: an R package for admixture graph manipulation and fitting. Bioinformatics. 2017;33(11):1738–40. doi: 10.1093/bioinformatics/btx048 28158333
59. Pfeifer B, Wittelsburger U, Ramos-Onsins SE, Lercher MJ. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol. 2014;31(7):1929–36. doi: 10.1093/molbev/msu136. 24739305; PubMed Central PMCID: PMC4069620.
60. Weir BS, Cockerham CC. Estimating F-Statistics for the Analysis of Population Structure. Evolution. 1984;38(6):1358–70. doi: 10.1111/j.1558-5646.1984.tb05657.x. 28563791.
61. Pembleton LW, Cogan NO, Forster JW. StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour. 2013;13(5):946–52. Epub 2013/06/07. doi: 10.1111/1755-0998.12129. 23738873.
62. Hill WG, Weir BS. Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol. 1988;33(1):54–78. Epub 1988/02/01. doi: 10.1016/0040-5809(88)90004-4 3376052.
63. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–5. Epub 2008/04/10. doi: 10.1093/bioinformatics/btn129. 18397895.
64. Goudet J. hierfstat, a package for r to compute and test hierarchical F-statistics. Molecular Ecology Notes. 2005;5(1):184–6. doi: 10.1111/j.1471-8286.2004.00828.x
65. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, et al. The Pfam protein families database. Nucleic acids research. 2004;32(Database issue):D138–D41. doi: 10.1093/nar/gkh121. 14681378.
66. Kessi-Perez EI, Araos S, Garcia V, Salinas F, Abarca V, Larrondo LF, et al. RIM15 antagonistic pleiotropy is responsible for differences in fermentation and stress response kinetics in budding yeast. FEMS Yeast Res. 2016. doi: 10.1093/femsyr/fow021. 26945894.
67. Hall BG, Acar H, Nandipati A, Barlow M. Growth rates made easy. Mol Biol Evol. 2014;31(1):232–8. doi: 10.1093/molbev/mst187. 24170494.
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