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

Nespolo, Roberto F.; Villarroel, Carlos A.; Oporto, Christian I.; Tapia, Sebastián M.; Vega-Macaya, Franco; Urbina, Kamila; Chiara, Matteo De; Mozzachiodi, Simone; Mikhalev, Ekaterina; Thompson, Dawn; Larrondo, Luis F.; Saenz‐Agudelo, Pablo; Liti, Gianni; Cubillos, Francisco A.

doi:10.1371/journal.pgen.1008777

Cited by 48 publications

(148 citation statements)

References 67 publications

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“…These strains were previously reported and belong to the Patagonia B cluster [27]. S. cerevisiae L299 [31] and MTF2444 (EC1118 hsp12::GFP) [32] strains were used as growth control and in the competition assays, respectively.…”

Section: Microorganisms and Culture Mediamentioning

confidence: 99%

“…The phenotyping assay was performed as previously described [27]. Briefly, isolates were pre-cultivated in 200 L 0.67% YNB medium supplemented with glucose 2% for 48 h at 25°C.…”

Section: Phenotyping Assaymentioning

confidence: 99%

“…Given the recent discovery of S. eubayanus, its puzzling origin and apparently coevolutionary association with Nothofagus trees, several authors have analyzed the worldwide distribution of S. eubayanus, together with its genetic, phenotypic, and fermentative diversity [24][25][26][27]. Patagonian isolates of S. eubayanus exhibit the most extensive genetic diversity, and the presence of the most significant number of lineages compared to Northern hemisphere populations, including five different lineages and a large .…”

Section: Introductionmentioning

confidence: 99%

“…CC-BY 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made The copyright holder for this preprint this version posted December 8, 2020. ; https://doi.org/10.1101/2020.12.07.415240 doi: bioRxiv preprint group of admixed isolates [26,27]. To date, there is no evidence of S. eubayanus isolates 97 in Europe, where the original S. pastorianus hybrid likely originated.…”

Section: Introductionmentioning

confidence: 99%

“…To date, there is no evidence of S. eubayanus isolates 97 in Europe, where the original S. pastorianus hybrid likely originated. Interestingly, 98 fermentation capacity varies significantly between S. eubayanus isolates, possibly due to 99 differences in maltose consumption and diauxic shift capacity, resulting in two opposite outcomes: successful or stuck fermentations [27]. These isolates produce fruit and floral flavors in beer [28], but high levels of 4-vinyl guaiacol, considered a phenolic off-flavor that provides a clove-like aroma, which is not preferred among consumers [21,28,29] [30].…”

Section: Introductionmentioning

confidence: 99%

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Rapid selection response to ethanol inS. eubayanusemulates the domestication process under brewing conditions

Mardones

Villarroel

Abarca

et al. 2020

Preprint

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Although the typical genomic and phenotypic changes that characterize the evolution of organisms under the human domestication syndrome represent textbook examples of rapid evolution, the molecular processes that underpin such changes are still poorly understood. Domesticated yeasts for brewing, where short generation times and large phenotypic and genomic plasticity were attained in a few generations under selection, are prime examples. To experimentally emulate the lager yeast domestication process, we created a genetically complex (panmictic) artificial population of multiple Saccharomyces eubayanus genotypes, one of the parents of lager yeast. Then we imposed a constant selection regime under a high ethanol concentration in 10 replicated populations during 260 generations (six months) and compared them with evolved controls exposed solely to glucose. Evolved populations exhibited a selection differential of 60% in growth rate in ethanol, mostly explained by the proliferation of a single lineage (CL248.1) that competitively displaced all other clones. Interestingly, the outcome does not require the entire time course of adaptation, as four lineages monopolized the culture at generation 120. Sequencing demonstrated that de novo genetic variants were produced in all evolved lines, including SNPs, aneuploidies, INDELs, and translocations. In addition, the evolved populations showed correlated responses resembling the domestication syndrome: genomic rearrangements, faster fermentation rates, lower production of phenolic-off flavors and lower volatile compound complexity. Expression profiling in beer wort revealed altered expression levels of genes related to methionine metabolism, flocculation, stress tolerance and diauxic shift, likely contributing to higher ethanol and fermentation stress tolerance in the evolved populations. Our study shows that experimental evolution can rebuild the brewing domestication process in “fast motion” in wild yeast, and also provides a powerful tool for studying the genetics of the adaptation process in complex populations.

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Section: Microorganisms and Culture Mediamentioning

confidence: 99%

“…The phenotyping assay was performed as previously described [27]. Briefly, isolates were pre-cultivated in 200 L 0.67% YNB medium supplemented with glucose 2% for 48 h at 25°C.…”

Section: Phenotyping Assaymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Rapid selection response to ethanol inS. eubayanusemulates the domestication process under brewing conditions

Mardones

Villarroel

Abarca

et al. 2020

Preprint

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Identification of new ethanol‐tolerant yeast strains with fermentation potential from central Patagonia

Villarreal

Quintrel

Olivares-Muñoz

et al. 2021

Yeast

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The quest for new wild yeasts has increasingly gained attention because of their potential ability to provide unique organoleptic characters to fermented beverages. In this sense, Patagonia offers a wide diversity of ethanol‐tolerant yeasts and stands out as a bioprospecting alternative. This study characterized the genetic and phenotypic diversity of yeast isolates obtained from Central Chilean Patagonia and analyzed their fermentation potential under different fermentative conditions. We recovered 125 colonies from Nothofagus spp. bark samples belonging to five yeast species: Saccharomyces eubayanus, Saccharomyces uvarum, Lachancea cidri, Kregervanrija delftensis, and Hanseniaspora valbyensis. High‐throughput microcultivation assays demonstrated the extensive phenotypic diversity among Patagonian isolates, where Saccharomyces spp and L. cidri isolates exhibited the most outstanding fitness scores across the conditions tested. Fermentation performance assays under wine, mead, and beer conditions demonstrated the specific potential of the different species for each particular beverage. Saccharomyces spp. were the only isolates able to ferment beer wort. Interestingly, we found that L. cidri is a novel candidate species to ferment wine and mead, exceeding the fermentation capacity of a commercial strain. Unlike commercial strains, we found that L. cidri does not require nutritional supplements for efficient mead fermentation. In addition, L. cidri produces succinic and acetic acids, providing a distinct profile to the final fermented product. This work demonstrates the importance of bioprospecting efforts in Patagonia to isolate novel wild yeast strains with extraordinary biotechnological potential for the fermentation industry.

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

Spurley

Fisher

Langdon

et al. 2021

Yeast

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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. Here, 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

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

Cited by 48 publications

References 67 publications

Rapid selection response to ethanol inS. eubayanusemulates the domestication process under brewing conditions

Rapid selection response to ethanol inS. eubayanusemulates the domestication process under brewing conditions

Identification of new ethanol‐tolerant yeast strains with fermentation potential from central Patagonia

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

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