Diversity and adaptive evolution of Saccharomyces wine yeast: a review Souhir Marsit, Sylvie Dequin To cite this version: Souhir Marsit, Sylvie Dequin. Diversity and adaptive evolution of Saccharomyces wine yeast: a review. FEMS Yeast Research, Oxford University Press (OUP), 2015, 15 (7), 12 p. 10.1093/femsyr/fov067. hal-01837757 HAL Id: hal-01837757 https://hal.archives-ouvertes.fr/hal-01837757 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. FEMS Yeast Research, 15, 2015, fov067 doi: 10.1093/femsyr/fov067 Advance Access Publication Date: 23 July 2015 Minireview MINIREVIEW Diversity and adaptive evolution of Saccharomyces wine yeast: a review Souhir Marsit1,2,3 and Sylvie Dequin1,2,3,∗ 1INRA, UMR1083, SPO, F-34060 Montpellier, France, 2Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France and 3Montpellier University, UMR1083, SPO, F-34060 Montpellier, France ∗ Corresponding author: Institut national de la recherche agronomique, Unite´ mixte de recherche Sciences pour l’œnologie, 2 place Viala, Montpellier, 34060, France. Tel: +33-4-99-61-25-28; Fax: +33-4-99-61-28-57; E-mail: [email protected] One sentence summary: This review summarizes current knowledge and recent advances on the diversity and evolutionary history of Saccharomyces cerevisiae wine yeasts, focusing on the domestication fingerprints identified in these strains. Editor: Jens Nielsen ABSTRACT Saccharomyces cerevisiae and related species, the main workhorses of wine fermentation, have been exposed to stressful conditions for millennia, potentially resulting in adaptive differentiation. As a result, wine yeasts have recently attracted considerable interest for studying the evolutionary effects of domestication. The widespread use of whole-genome sequencing during the last decade has provided new insights into the biodiversity, population structure, phylogeography and evolutionary history of wine yeasts. Comparisons between S. cerevisiae isolates from various origins have indicated that a variety of mechanisms, including heterozygosity, nucleotide and structural variations, introgressions, horizontal gene transfer and hybridization, contribute to the genetic and phenotypic diversity of S. cerevisiae. This review will summarize the current knowledge on the diversity and evolutionary history of wine yeasts, focusing on the domestication fingerprints identified in these strains. Keywords: evolutionary history; comparative genomics; wine fermentation; domestication; horizontal transfer; hybrids INTRODUCTION visiae wine yeasts have attracted considerable interest in recent years. Although Saccharomyces cerevisiae is a well-studied model that Wine has a long and rich history, dating back thousands of has aided our understanding of eukaryotic cellular processes years, closely associated with the history of agriculture. The ear- and was the first eukaryotic genome to be completely sequenced liest archaeological evidence for the production of a fermented (Goffeau et al. 1996), this yeast has only recently been established beverage made of a mixture of rice, honey and fruit is in China as a model for studies in ecological and evolutionary genetics dated to 7000 BC (McGovern et al. 2004). The first chemical ev- (Landry et al. 2006). Some authors have defended that its clos- idence of the presence of wine is dated to 5400–5000 BC, from est relative S. paradoxus is a better model for ecology and evo- the Neolithic period site called Hajji Firuz in Iran, where the lutionary biology because it is not associated with humans (Re- presence of combined calcium salt from tartaric acid and tere- plansky et al. 2008). However, S. cerevisiae is not domesticated as binth resin was identified in a pottery jar (McGovern, Donald a whole and population genetics analysis of both domesticated and Glusker 1996). Evidence that S. cerevisiae was probably re- and a growing number of wild isolates is continuously offering sponsible for wine fermentation in Egypt by at least 3150 BC was new insights into the ecological distribution, population struc- provided (Cavalieri et al. 2003). Wine fermentation technologies ture and biogeography of this species. In this context, S. cere- expanded from Mesopotamia towards Europe and subsequently Received: 10 May 2015; Accepted: 10 July 2015 C FEMS 2015. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 2 FEMS Yeast Research, 2015, Vol. 15, No. 7 spread to the New World (McGovern 2003). Alcoholic fermenta- piratory genes (Postma et al. 1989; Alexander and Jeffries 1990). tion is not only an efficient method for the preservation of the However, the immediate occurrence of alcoholic fermentation quality and safety of beverages and foods, but wine is also a after the addition of sugar to sugar-limited and respiratory cul- widespread drug and medicine of antiquity, reflecting the anal- tures, called the short-term Crabtree effect, has been attributed gesic, disinfectant and preservative properties of this alcoholic to an overflow in sugar metabolism (Pronk, Steensma and Van beverage. Over time, wine has influenced geography, economics, Dijken 1996; Vemuri et al. 2007). It has recently been suggested archeology, history, mythologies and religions, arts and tradi- that overflow metabolism is the fundamental mechanism be- tions, law and medicine. Today, this beverage has a unique place hind both long- and short-term Crabtree effect, which originated in most societies, with tremendous economic and cultural value. approximately 125–150 million years ago (Mya) in the Saccha- It was not until 1860 that Louis Pasteur discovered the ori- romyces lineage (Hagman and Piskurˇ 2015). Overflow metabolism gin of fermentation and the implication of yeast (Pasteur 1860). was first acquired, providing a general strategy to increase en- In the early 1880s, Emile Christian Hansen, from the Carlsberg ergy production rates and enabling rapid glucose consump- laboratory in Denmark, developed the first pure yeast culture tion. The glucose-mediated repression of respiration would have and wort inoculation was performed some years later. In 1890, been acquired as a second step to further increase overflow and Muller-Thurgau¨ performed the first inoculation of a grape must ethanol production, thereby inhibiting the growth of other mi- with a pure yeast culture. Surprisingly, this practice was effec- crobes. This characteristic is primarily confined among S. cere- tively used in oenology only in the 1970s, almost one century visiae and closely related species that diverged after whole- later. After the 1970s, these practices were generalized and cur- genome duplication, less than 100 Mya (Hagman and Piskurˇ rently most wine fermentations worldwide use selected starter 2015). yeasts primarily belonging to S. cerevisiae. These practices have Saccharomyces and Dekkera are characterized by a ‘make- improved the control and reliability of the fermentation process, accumulate-consume’ strategy, as these yeasts also efficiently limiting microbiological alterations and have largely contributed catabolize ethanol. This strategy could confer an advantage to increased wine quality in recent decades. Consistently, most to these species in nature, as these yeasts rapidly consume a pioneering research in the genetics, genomics, physiology and high quantity of sugars, transforming these carbohydrates into evolutionary biology of wine yeasts has been developed in S. cere- ethanol, which inhibits the growth of other species, and subse- visiae and to a lesser extent on other Saccharomyces species and quently consuming ethanol after establishing competitive dom- hybrids prominent in the wine industry. This review will focus inance within the ecological niche (Thomson et al. 2005;Piskurˇ on the most recent advances on the history, diversity and evo- et al. 2006; Rozpedowska et al. 2011;Dashkoet al. 2014). lution of Saccharomyces wine yeasts. The make-accumulate-consume strategy emerged after the split between the S. cerevisiae and Kluyveromyces lactis lineages approximately 100 Mya, suggesting that this process reflected SACCHAROMYCES AND THE the appearance of modern plants with fruits, which occurred MAKE-ACCUMULATE-CONSUME STRATEGY >125 Mya, far earlier than the human domestication of yeast (Thomson et al. 2005;reviewedinPiskurˇ et al. 2006). Comparative The fermentation of grape musts can spontaneously oc- genomics approaches revealed that at least two mechanisms cur through the activity of various microorganisms naturally might be involved in the acquisition of this capacity. Thomson present on grape berries. More than 40 yeast species have et al. (2005) reconstructed an ancestral Saccharomyces alcohol de- been identified from grape must (reviewed in Jolly, Varela and hydrogenase gene (ADH) and showed that the pre-duplication Pretorius 2014),