An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages

• DOI: 10.1371/journal.pgen.1008777
• Publication Date: 2020-05-01T17:32:34Z
• Authors: Roberto F. Nespolo; Carlos A. Villarroel; Christian I. Oporto; Sebastián M. Tapia; Franco Vega-Macaya; Kamila Urbina; Matteo De Chiara; Simone Mozzachiodi; Ekaterina Mikhalev; Dawn Thompson; Luis F. Larrondo; Pablo Saenz-Agudelo; Gianni Liti; Francisco A. Cubi...
• Keywords: Gene Flow; 0301 basic medicine; 13 Climate Action; 570; Whole Genome Sequencing; Acclimatization; Argentina; Genetic Variation; QH426-470; 15. Life on land; [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology; Cold Temperature; Phylogeography; Saccharomyces; 03 medical and health sciences; 13 Acción por el clima; [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN]; Genetics; [SDV.BBM.GTP] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN]; Chile; Genome, Fungal; [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology; Phylogeny; Research Article

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.