Received: 1 March 2018 Revised: 7 May 2018 Accepted: 7 May 2018 DOI: 10.1002/yea.3350 ECOYEAST REVIEW Bakery yeasts, a new model for studies in ecology and evolution Belén Carbonetto1,2* | Johan Ramsayer1* | Thibault Nidelet1 | Judith Legrand3 | 1 Delphine Sicard 1 SPO, Univ Montpellier, INRA, Montpellier SupAgro, Montpellier, France Abstract 2 Yeasts have been involved in bread making since ancient times and have thus played Instituto Gulbenkian de Ciência, Bioinformatics and Computational Biology Unit, Oeiras, Portugal 3 GQE‐Le Moulon, INRA, Univ. Paris‐Sud, CNRS, AgroParisTech, Université Paris‐Saclay, Gif‐sur‐Yvette, France Correspondence Delphine Sicard, SPO, Univ Montpellier, INRA, Montpellier SupAgro, Montpellier, France. Email: delphine.sicard@inra.fr Funding information Fonds de dotation EKIP; Agence Nationale de la Recherche, Grant/Award Number: ANR‐13‐ ALID‐0005 an important role in the history and nutrition of humans. Bakery‐associated yeasts have only recently attracted the attention of researchers outside of the bread industry. More than 30 yeast species are involved in bread making, and significant progress has been achieved in describing these species. Here, we present a review of bread‐ making processes and history, and we describe the diversity of yeast species and the genetic diversity of Saccharomyces cerevisiae isolated from bakeries. We then describe the metabolic functioning and diversity of these yeasts and their relevance to improvements in bread quality. Finally, we examine yeast and bacterial interactions in sourdoughs. The purpose of this review is to show that bakery yeast species are interesting models for studying domestication and other evolutionary and ecological processes. Studying these yeasts can contribute much to our fundamental understanding of speciation, evolutionary dynamics, and community assembly, and this knowledge could ultimately be used to adjust, modify, and improve the production of bread and the conservation of microbial diversity. KEY W ORDS Kazachstania, microbial community, sourdough microbiota, yeast‐bacteria interaction, yeast domestication 1 | HISTORY PROCESSES OF BR E A D AND BA K I N G evidence for leavened breads was found during classic antiquity in the Leavened bread results from the activity of gas‐producing microorganisms, which produce gas pockets in the baked product. The raw materials are milled cereal, water, and fermentative yeast and/or bacteria. Additional components can be included in certain cultural traditions, where honey, fruits, nuts, and diverse plant seeds can be sources of other microorganisms and an additional substrate for microbial activity. Bread is one of the most ancient and widespread fermented food products. The history of fermented products dates back to the Neolithic period, when plant and animal domestication occurred (Diamond, 2002; Gibbons & Rinker, 2015; McGovern, 2009; McGovern, 2013; *Belen Carbonetto and Johan Ramsayer should be considered joint first authors. Yeast. 2018;35:591–603. Salque et al., 2013; Sicard & Legras, 2011). The earliest archaeological second millennium BCE in Egypt (Samuel, 1994; Samuel, 2002) and the first millennium BCE in North Western China (Shevchenko et al., 2014). In Egypt, optical and scanning electron microscopy revealed the presence of yeast cells in bread loaves recovered from tombs (Samuel, 1996). In China, proteomics analysis was used to identify proteins found in ancient food pieces retrieved from the Subeixi cemetery. Proteins were found to belong to cereals, to yeasts of the Sacharomycetaceae family, to lactic acid bacteria (LAB) from the Leuconostocaceae family, to Lactobacillus families, and to humans (Shevchenko et al., 2014), allowing for the hypothesis that the analysed food pieces belonged to leavened bread. However, the origin of the microbial inoculum in ancient bread is not clear. It is still wileyonlinelibrary.com/journal/yea © 2018 John Wiley & Sons, Ltd. 591 CARBONETTO 592 unknown whether yeast cells dispersed from neighbouring natural environments (such as cereals, soil, or trees) or fermented beverages or whether the inverse process occurred. Archaeological evidence for fermented beverages predates that for bread (McGovern, 2013), Outstanding questions about yeast domestication and ecology in the bread‐making environment but this finding might be related to the higher conservation ability of alcoholic beverages in pottery compared with cooked—and often burnt—bread remains. The art of making leavened bread developed during ancient and What is the impact of human practice on the evolution of bakery yeasts? Although bread is of historical and cultural importance medieval ages and was disseminated throughout the Mediterranean worldwide, the domestication of its associated microbial and in Middle Eastern countries. Until the Middle Ages, bread was communities is not yet completely understood. The mostly made within the home. During the population expansion of domestication of yeasts likely started in Egyptian times and the 11th and 12th centuries, communal mills and ovens were con- is ongoing every time a baker starts a new sourdough. It is structed, making the bread process a part of the social organization difficult to use palaeogenomics on ancient bread because of of the community. Professional bakers became common. Bread mak- the technical difficulties of amplifying DNA from burnt or ing consisted of mixing flour, water, and sourdough. Sourdough was heated bread materials. However, ongoing domestication made of flour and water and contained fermenting yeast and LAB. can be studied using experimental evolution induced in the These microorganisms came from the flour, water, and/or other laboratory or in bakeries. A better understanding of bread‐making environments. Depending on the geographic location microbial domestication through an analysis of ongoing and cultural habits, different kinds of cereal flours were used, including selection and bread‐making practices will shed light on the wheat, barley, emmer, einkorn, khorasan, rye, spelt, teff, maize, or sor- rate of domestication and impact on the sustainability of the ghum (Mondal & Datta, 2008; Samuel, 2002). bakery food chain. In the 19th century, the industrialization of food production and the advent of microbiology as a science resulted in changes in yeast starters (Gélinas, 2010). This development changed bread pro- How have bakery yeasts dispersed, and what is the level of gene transfer between yeasts isolated from bakeries and from neighbouring environments? duction and baking dramatically. The consequences of this change Bakers may use commercial yeasts and/or spontaneously are apparent in modern times, where most bread is made using the fermented sourdough. Sourdough can be seen as a sink for commercial baker's yeast Saccharomyces cerevisiae. Using one selected microbes coming from the air, cereals, and water. Analysing strain of a single species of yeast provides industrial control and repro- dispersal along the bakery food chain from the soil to ducibility in the baking process. Commercially available sourdoughs bread as well as studying gene transfer between strains containing the selected yeasts and LAB strains with specific and desir- from different natural environments and bakery strains of able baking characteristics are also available. Usually, these sour- sourdough and commercial origins will shed light on yeast doughs, which are also called sourdough starters, are chosen by dispersion and the impact of humans on yeast evolution. bread‐making practices (Blandino, Al‐Aseeri, Pandiella, Cantero, & Webb, 2003; Roussel & Chiron, 2005). The possibility of making pure cultures and drying yeast cells led to the development of industrial bakers for the characteristics they provide to the final bread product, such as flavour and aroma (Hansen & Schieberle, 2005). However, in modern times, bread is still made traditionally using natural sourdough, which is often spontaneously fermented (Figure 1; Hammes & Gänzle, 1997). By spontaneously, we mean that no commercial starters are added during the sourdough making process. Sourdough is initiated What is the overall functional diversity among and within bakery yeast species? Can we detect signatures of selection through phenotypic convergence and population genomics studies? by mixing flour and water and eventually adding other ingredients, The functional diversity of yeast species found in sourdough such as fruits or honey. After one or a few days, flour and water are has not been well described beyond that of Saccharomyces added in order to maintain the fermentation process. The addition of cerevisiae. Analysing phenotypic variation among and within flour and water is called backslopping. The process is repeated until yeast species, together with genomic analysis, will enable the sourdough is considered to be ready for making bread. The chief the detection of selection signatures and the targeting and (or mother) sourdough is then mixed with flour and water to make a construction of interesting strains for the bakery industry. final sourdough to be added to the bread dough during kneading. A piece of final sourdough or dough after kneading is then put aside for the next bread‐making process. Sourdough is therefore maintained by continuous reinoculation of new batches of flour and water, that is, backslopping. In ecology, this process can be seen as a source–sink dynamic model, where sourdough is the sink and flour, air, water, the baker's hands, added sugar sources, such as fruit or honey, or added yeasts starters are the source. In evolution, sourdough can be Can we find general rules that govern the interactions between yeast and bacteria? Can we predict the outcome? The sourdough ecosystem is remarkable in that it is a dynamic coexistence of several species of yeasts and bacteria. Daily feeding of fresh flour and water during ET AL. CARBONETTO ET AL. 593 bakery operations means that this ecosystem exists over sourdough, more specifically in France: https://www6.inra.fr/bakery_ time and in some cases, over hundreds of years. eng) using classical microbiological methods as well as new methods The interaction between yeast and bacteria may result of metabarcoding and metagenomics sequencing. In some cases, sour- from coevolution and dough may also contain deliberately added yeast starters, which may is likely ruled by metabolic may remain in the sourdough from one batch to the next. In most cases, influence the structure and composition of sourdough the literature does not document whether yeast starter has been microbial mechanisms, added in the analysed sourdough. In addition, the literature is mostly intraspecific and interspecific variations are observed, concerned with sourdough diversity from China, Tibet, Italy, and Bel- which make studying them challenging. Nevertheless, as gium. Citizen science projects are considerably increasing the sampling the microbial communities of sourdough are rather simple, area and diversity. Unfortunately, the results of these projects are not they represent a good model for studying community yet published, but they are shown with open access on geographic assembly rules. maps on their internet website over the world: (http://robdunnlab. exchanges. Several mechanisms communities. For of interaction several com/projects/sourdough, and more specifically in France: https:// www6.inra.fr/bakery_eng). Rob Dunn's lab website presents yeast species diversity in more than 500 sourdoughs collected all over the seen as an ongoing experimental evolution in batch culture, where world, including homemade sourdoughs. The bakery project presents fresh medium (flour and water) is regularly added to allow ongoing yeast species diversity found in sourdoughs collected in France from population growth. bakers with diverse bread‐making practices and using organic flours. Overall, these projects will allow us to better analyse geographic structuration and human impacts on yeast species diversity. 2 | Y E A S T D I V E R S I T Y I N T H E B R E A D‐ MAKING PROCESS 2.1 | The sourdough microbial community Over 30 yeast species and 50 species of LAB have been identified in sourdoughs (De Vuyst et al., 2014; De Vuyst et al., 2016; Jacques et al., 2016; Lhomme et al., 2015; Lhomme et al., 2016; Liu et al., 2018). Yeast species primarily contribute to the leavening and aroma compound of sourdough bread (De Vuyst, Van Kerrebroeck, & Leroy, The diversity of microorganisms found in sourdoughs throughout the 2017). LAB species are mostly responsible for acidification but can world has been well described in both academic research (De Vuyst also et al., 2014; De Vuyst, Harth, Van Kerrebroeck, & Leroy, 2016) and (heterofermentative LAB; De Vuyst et al., 2017). Usually, the participatory intrasourdough species diversity (alpha diversity) is low with a single research projects (http://robdunnlab.com/projects/ participate to flavour formation and dough leavening FIGURE 1 Steps in sourdough bread‐making process. Usually, a chief sourdough is used. This sourdough is created by mixing flour and water and maintained by continuous backslopping. New additions of flour and water lead to the final sourdough, which is used for bread making. The final sourdough is mixed with flour, water, and other ingredients (salt, seeds, yeasts starters, etc.) during kneading to give the dough. The dough is then left to rise. During this first fermentation step, yeast cells divide. The gluten proteins form a network in which the carbon dioxide produced from the breakdown of carbohydrates (starch and sugars) remains. After this first step of fermentation, the dough is shaped into a loaf, which is set aside for a second step of fermentation. Then, the loaf is cooked. For the next bread‐making process, a piece of the final sourdough or a piece of dough taken after kneading becomes the chief sourdough (dashed arrows) [Colour figure can be viewed at wileyonlinelibrary.com] CARBONETTO 594 ET AL. dominant yeast species and a dominant LAB species (De Vuyst et al., the sourdough (Figure 2b). Most yeast species found in sourdough 2014; Vogel, Mueller, Stolz, & Ehrmann, 1996). In contrast, the were detected in wheat sourdough, but this finding may be due to between‐sourdough species diversity (beta diversity) is relatively high. the larger number of studies performed on wheat sourdough. Among LAB, Lactobacillus plantarum, Lactobacillus fermentum, Yeast species diversity in sourdough has been well described in Lactobacillus paralimentarius, Lactobacillus plantarum, and Lactobacil- Italy, Belgium, and France (Figures 2 and 3, Table S1). We analysed lus sanfranciscensis are common (De Vuyst et al., 2014). Among the data obtained for 97 wheat sourdoughs (including possibly also yeasts, S. cerevisiae is the most commonly described dominant other cereals) described individually (Almeida & Pais, 1996; Corsetti species; however, it is absent in some cases, or it is found at low et al., 2001; Decimo, Quattrini, Ricci, Fortina, & Express, 2017; Desiye frequencies when other yeast species dominate. Other described & Abegaz, 2013; Foschino, Gallina, Andrighetto, Rossetti, & Galli, yeast species belong to the genus Saccharomyces (formerly sensu 2004; Gabriel, Lefebvre, Vayssier, & Faucher, 1999; Garofalo, Silvestri, stricto complex; Saccharomyces uvarum, Saccharomyces bayanus), to Aquilanti, & Clementi, 2008; Gatto & Torriani, 2004; Infantes & the neighbouring genus Kazachstania, and to the more genetically Schmidt, 1992; Lacumin et al., 2009; Lattanzi et al., 2013; Lhomme distant genera Pichia, Candida, Torulaspora, and Wickerhamomyces et al., 2015; Lhomme et al., 2016; Mäntynen et al., 1999; Minervini, (Figure 2, Table S1). Cagno, et al., 2012; Minervini, Lattanzi, et al., 2012; Minervini et al., The yeasts S. cerevisiae, Wickerhamomyces anomalus, Torulaspora 2015; Obiri‐Danso, 1994; Osimani et al., 2009; Pulvirenti, Caggia, delbrueckii, Pichia kudriavzevii, Kazachstania exigua, and Kazachstania Restuccia, Gullo, & Giudici, 2001; Saeed Anjum, Zahoor, Nawaz, & humilis are the most geographically widespread species in sourdoughs Sajjad‐Ur‐Rehman, 2009; Salovaara & Savolainen, 1984; Scheirlinck (Figure 2a). All six species have been found in sourdough samples from et al., 2007; Spicher & Schröder, 1978; Succi et al. 2003; Vrancken Asia and Europe, and some of them have also been found in America, et al., 2010; Valmorri, Tofalo, Settanni, Corsetti, & Suzzi, 2010; Zhang Africa, and Australia (Figure 2a, and see links for interactive maps et al., 2015; Zhang et al., 2011). S. cerevisiae was found to be present, describing http:// but not necessarily dominant, in almost 80% of the sourdoughs robdunnlab.com/projects/sourdough/map and https://www6.inra.fr/ (Figure 3). K. humilis and W. anomalus were respectively present in bakery_eng/Results). All of these species' genomes, except for the 16% and 8% of these sourdoughs. The 10 remaining species where two Kasachstania species, have been sequenced (Chan, Gan, Ling, & present in less than 5% of the sourdoughs, and six species were only Rashid, 2012; Goffeau et al., 1996; Gomez‐Angulo et al., 2015; Gor- documented in one of the studies. The species W. anomalus was found yeast species composition per sourdough don et al., 2011; Park et al., 2018; Riley et al., 2016; Wolfe et al., in Belgium but not in France or Italy, and the species Kazachstania 2015; Wu, Buljic, & Hao, 2015). The distribution of these species did bulderi was detected only in France. However, it is not clear whether not appear to be correlated with the type of cereal used to make there is a geographic structure to the distribution of yeast species (a) (b) FIGURE 2 Phylogeny and presence of yeast species in worldwide sourdough samples, as documented in the scientific literature. The genetic relationships of yeast species are based on a parsimony analysis of 664 sites of the D1/D2 LSU rDNA region. Bootstrap support reveals the low power of the D1/D2 LSU rDNA region for analysing the phylogeny of this set of yeast species. The distribution of each yeast species is shown (a) according to the country of origin and (b) according to the flour used. Black squares represent presence. The references used for this figure were retrieved from the review by De Vuyst et al., 2016, and updated (Table S1). No meta‐analysis was carried out. Note that the distribution of yeast species also reflects biases in sampling in the literature. For instance, Saccharomyces cerevisiae was found in North American sourdoughs in the citizen science project CARBONETTO ET AL. 595 FIGURE 3 The frequency of yeast species among 97 European wheat sourdough samples (a) over all countries and (b) broken down by country. The frequency was calculated by counting the number of sourdoughs carrying the species over the total number of sourdoughs. Thus, a high frequency does not necessarily imply dominance within the sourdough because sourdough collections were done in different kinds of baker- have been found in North American and European sourdoughs ies with no detailed documentation of bakery practices. Thus, there (Lhomme et al., 2015; Lhomme et al., 2016; De Vuyst et al., 2016 may be a confounding effect between countries and bread production but see also http://robdunnlab.com/projects/sourdough/map and strategies (conventional/artisanal bakeries, organic/nonorganic baker- https://www6.inra.fr/bakery_eng/). In addition, K. exigua has been ies, starters used or not). Moreover, the number of strains analysed for detected in Asia, Australia, and Africa, whereas K. humilis has been each sourdough and the yeast species identification methods varied detected in Asia, Australia, Africa, and Oceania (Figure 2, see also among studies. Intensive collection of samples prepared by standard- http://robdunnlab.com/projects/sourdough/map/). ized methods in the context of well‐characterized sociological/anthro- observed differences in the geographic distribution of Kazachstania pological bakery practices is needed to better understand how species may reflect differences in species frequency but also uneven- geographic distributions, population structures, and the influence of ness in sampling efforts. domestication impact the diversity of bakery yeast species. However, the K. exigua is the most frequently cited sourdough species in the literature and is most commonly found in yeast strain collections. It is 2.2 | Genus Kazachstania the first species to have been isolated from a sourdough (in San Francisco, Sugihara, Kline, & Miller, 1971). It has also been isolated The genus Kazachstania is the closest neighbour to the genus Saccha- from natural habitats, such as soil, mangroves, and fruit, and from sev- romyces, which contains S. cerevisiae. It contains 44 species that can eral fermented products, such as grape must, kimchi, kefir, and dairy. be found in diverse habitats, such as soil, animals, water, and The LSU D1/D2 rRNA gene sequence does not discern species fermented products (Gordon et al., 2011; Jacques et al., 2016; James assigned to the genus Kazachstania, especially among species close et al., 2015; Kabisch et al., 2016; Kurtzman & Robnett, 1998; to K. exigua (Jacques et al., 2016, Figure 2). The ITS rRNA gene Kurtzman et al., 2005; Kurtzman, Fell, & Boekhout, 2011; Kurtzman sequence is more divergent, but it may also not be sufficient for dis- & Robnett, 2003; Lee, Yao, Liu, Young, & Chang, 2009; Limtong, criminating between species in some cases (Jacques et al., 2016). It Yongmanitchai, Tun, Kawasaki, & Seki, 2007; Lu, Cai, Wu, Jia, & is then possible that several erroneous identifications have occurred Bai, 2004; Nisiotou & Nychas, 2008; Safar, Gomes, Marques, in past studies, and therefore, organisms classified as K. exigua may Lachance, & Rosa, 2013; Wu & Bai, 2005). Seven species have been actually represent a complex of closely related species. isolated from sourdoughs. It is therefore the best represented genus The phylogenetic relationships between Kazachstania species in sourdough (see Figure 2 for a phylogeny of species found in sour- remain poorly resolved because only three complete, well‐assembled dough). New members of the genus Kazachstania are being discov- genomes are available. These genomes include those of Kazachstania ered by the help of barcoding regions, such as ITS and the large africana, which is 11 Mb and includes over 12 chromosomes, subunit rRNA gene, which allows for better circumscription of the Kazachstania naganishii, which is 10.8 Mb and has over 13 chromo- genus as a clade (Alvarez‐Perez et al., 2012; Araújo et al., 2012; somes (Gordon et al., 2011; Wolfe et al., 2015), and K. saulgeensis, Cardinali et al., 2012; Chen, Wei, Jiang, Wang, & Bai, 2010; Jacques which is 12.9 Mb and has over 17 scaffolds (Sarilar et al., 2017). These et al., 2016; James et al., 2015; Kabisch et al., 2013; Suh & Zhou, three species were isolated from soil, decaying leaves, and sourdough, 2011). Recently, Kazachstania saulgeensis was discovered in French respectively. Other Kazachstania genomes are currently being sourdoughs (Jacques et al., 2016). Kazachstania species found in sequenced and will assist in determining the phylogeny of the genus, sourdough occupy distant positions within the clade, although the which should lead to a better understanding of the genomic events phylogenetic relationship of Kazachstania species is not well resolved associated with yeast domestication and species radiation. yet (Figure 2). So far, two groups of sourdough species were defined. The first group contains Kazachstania barnettii, Kazachstania exigua, K. saulgeensis, K. bulderi, and K. humilis, and the second group harbours Kazachstania unispora and Kazachstania servazzi (Figure 2). 2.3 | Tracking the evolutionary history of S. cerevisiae found in bakeries K. unispora, K. servazzi, K. barnettii, and K. bulderi are less fre- S. cerevisiae, known as baker's yeast, is the most common yeast spe- quently detected as dominant species in sourdough. These species cies found in bread. It has been used as a starter since the 19th CARBONETTO 596 ET AL. century and is also the most frequent yeast species found in sour- some bakery strains of S. cerevisiae are tetraploids derived from the doughs, as described above. However, the literature has focused pri- hybridization of different S. cerevisiae diploid strains. These autotetra- marily on its importance in bread making and rarely on the ecology ploids are reproductively isolated from S. cerevisiae diploids and there- and evolution of S. cerevisiae strains from bakeries. fore represent new species, as defined by the biological species The population structure of S. cerevisiae strains from other habi- concept (Albertin et al., 2009). We have recently analysed a collection tats has already been studied. Strains isolated from soil, bark, fruits, of 330 bakery strains isolated worldwide and found that 75% of the fermented beverages, and vectors, such as Drosophila, bees, wasps, commercial bakery strains and 57% of the strains isolated from natural or humans, have been studied at the genetic level (Goddard & Greig, sourdoughs are tetraploids (Unpublished data). An analysis of their 2015; Jouhten, Ponomarova, Gonzalez, & Patil, 2016). Recently, genetic diversity is underway and will shed light on the history of whole genome studies comparing tens, hundreds, and now thousands S. cerevisiae bakery strains. of strains from natural and man‐made environments have emerged and provided insights into yeast domestication (Almeida et al., 2015; Fay & Benavides, 2005; Gallone et al., 2016; Gonçalves et al., 2016; Legras et al., 2018; Libkind et al., 2011; Liti et al., 3 | F U N C T I O N A L D I V E R S I T Y OF YE A S T S F OU N D I N SOU RD O U GH S A N D ST A R TE R S 2009; Ludlow et al., 2016; Peter et al., 2018; Schacherer, Shapiro, Ruderfer, & Kruglyak, 2009). Yeasts from wine, sake, cocoa, coffee, and beer have undergone various domestication events. Although 3.1 | Fermentation and use of sugar sources wine and sake strains were found to be monophyletic, beer strains Dominant yeast species in sourdoughs can ferment, that is, they have were polyphyletic. No geographical pattern was found for wine the ability to convert sugar into ethanol and carbon dioxide, under strains, but the genetic clustering of beer, cocoa, and coffee strains both anaerobic and aerobic conditions (Hagman, Säll, Compagno, & appears to be partly structured according to the geographic origin Piskur, 2013; Kurtzman et al., 2011). These yeasts are therefore of the isolates. Unfortunately, only a limited number of bakery strains Crabtree positive. were included in these population genomic studies, and thus, the In dough, there are three sources of sugar: (a) the sugars naturally domestication of bakery yeast strains remains to be analysed. The present in flour (including glucose, sucrose, fructose, and maltose), (b) most complete study is the recent genomic analysis of 37 bakery the sucrose that bakers may add, and (c) the maltose released by the strains in the 1002 Yeast Genomes Project (Peter et al., 2018). Most amylolytic breakdown of starch. Starch in wheat flour is usually dam- bakery strains clustered separately from the well‐defined wine and aged due to the milling process, allowing it to swell in water and be sake lineages, suggesting a distinct evolutionary history (Peter et al., readily hydrolysed by α‐amylase (Delcour et al., 2010). The source of 2018). Thirty‐one strains were found to cluster into two groups, amylase is the grain itself, but sometimes, bakers can also add fungal one of mixed origins and another of mosaic strains. These groups α‐amylase to the flour mix (Delcour et al., 2010; Kim, Kim, Yun, & also contained strains from diverse environments, such as trees, soil, Kim, 2016). Because maltose represents an important carbon source, insects, fruits, flowers, humans, water, and beer. The remaining six the ability to ferment maltose is directly linked to fermentation perfor- bakery strains joined the wine (two strains from Italy and Australia), mance (time and CO2 production) in dough. The fermentative capacity African beer (three strains from Ghana maize sourdough), and Asian of S. cerevisiae from bakery and nonbakery sources has been tested in fermentation (one industrial strain from Northern Europe) clusters. synthetic dough medium that mimics major bread dough types (Bell, Therefore, the bakery strains do not form a single separate group like Higgins, & Attfield, 2001). Bakery commercial strains were found to wine strains, suggesting that they have undergone several different have a better maltose‐utilizing capacity than strains from other domestication trajectories. Indeed, as they belong to different sources, suggesting an adaptation of commercial yeast to the dough groups, the data suggest that bakery strains have diverse origins. In environment. addition, part of them belong to a group of mosaic strains suggesting When glucose and fructose are available, maltose‐utilization they may have resulted from hybridization or gene flows between enzymes are repressed by catabolite repression (Gancedo, 1998; strains from diverse origins, such as beer, humans, and natural envi- Pacheco et al., 2012). This repression is critical for fermentation length ronments. Whether commercial bakery strains have escaped to the as it causes a lag phase in CO2 production until the genes encoding for wild and if sourdough strains have their origin in the wild remain the maltose‐utilization pathway are induced (Higgins et al., 1999). This unknown. The impact of human selection on the evolution of bakery reason is why the ability to ferment maltose at a high speed has S. cerevisiae strains still needs to be studied. always been a desirable feature in S. cerevisiae strain selection. A com- Bakery strains of S. cerevisiae are mostly polyploids. An intensive parison of S. cerevisiae and the closely related wild species Saccharo- study of the genetic diversity among 651 domesticated S. cerevisiae myces paradoxus showed a higher performance on maltose by the strains from 56 different geographical origins revealed that approxi- S. cerevisiae strains, suggesting that this feature may have been mately 50% of beer and bakery strains exhibited four alleles at several selected during the domestication of S. cerevisiae (Warringer et al., microsatellite loci, suggesting polyploidization and aneuploidization 2011). The genes involved in maltose utilization in S. cerevisiae are rep- events in the evolutionary history of these strains (Legras, Merdinoglu, resented in five well‐described MAL loci located on subtelomeric Cornuet, & Karst, 2007). This finding was later confirmed by the regions (Charron, Read, Haut, & Michels, 1989; Naumov, Naumova, genetic analysis of the karyotype, DNA content, and segregation of & Michels, 1994). The presence of just one MAL locus is sufficient bakery strains (Albertin et al., 2009). This analysis demonstrated that to allow maltose fermentation in Saccharomyces (Needleman, 1991; CARBONETTO ET AL. 597 Needleman et al., 1984). Each locus consists of a cluster of at least according to phenotypes suited for bread production. Strains are three different genes encoding maltose permease (MALT) and maltase selected for their fermentation performance and their ability to gener- (MALS) as well as the transcriptional activator for these genes (MALR). ate flavour and aroma compounds, such as alcohols, aldehydes, esters, The evolutionary history of the MALS genes has been well stud- ketones, and acid compounds, and to increase nutritional value. Other ied. The MALS gene is duplicated in modern strains, and the different desirable characteristics include biomass production, cell growth rate, copies have diverged to enable growth on different disaccharides. dehydration, and cold stress‐tolerance (Oda & Ouchi, 1989; Randez‐ Some paralogues have retained the ancestral preference for maltase Gil, Córcoles‐Sáez, & Prieto, 2013). This selection process has led to activity, whereas others have specialized towards a novel specificity the existence of high diversity in industrial strains (Randez‐Gil et al., for isomaltose (Brown, Murray, & Verstrepen, 2010; Voordeckers 2013). Commercial yeast providers and scientists are testing the et al., 2012). The MALS ancestral duplication appears to postdate potential of other species or strains on the design of new bakery the divergence between the Kluyveromyces and Saccharomyces clade yeasts and sourdough starters (Aslankoohi et al., 2016; Pacheco (150 Mya) and predate the divergence between Lachancea and Sac- et al., 2012; Plessas, Bekatorou, et al., 2008; Plessas, Fisher, et al., charomyces and the yeast whole genome duplication event (80 Mya). 2008; Steensels et al., 2014; Zhou et al., 2017). It is tempting to speculate that the duplication and diversification of MALS genes has enabled yeast colonization of new niches made available by the appearance of fruiting plants from angiosperms. However, this speculation must be made with caution. Modern MAL locus duplications and deletions may be a result of yeast domestication. MAL genes are amplified in beer and sake‐related strains, which grow in maltose‐rich media, whereas they are often missing in wine strains, which grow in maltose‐free grape must (Gallone et al., 2016). Unfortunately, the evolution of the MAL gene family has not yet been studied in S. cerevisiae bakery strains. The characterization of maltose utilization by osmotolerant strains of T. delbrueckii has been studied (Alves‐Araújo et al., 2007). The results have shown an apparent coregulation of maltose transport and maltase activity, both being subject to glucose repression and induction by maltose. Catabolite repression by glucose control was 3.2.1 | Fermentation performance Among other yeast species, K. humilis may be a good candidate for the generation of new sourdough starters. Differences in the carbon utilization profiles and leavening capacity of K. humilis sourdough strains have been evaluated (Häggman & Salovaara, 2008a; Vigentini et al., 2014). K. humilis strains have shown a higher leavening capacity than S. cerevisiae strains isolated from sourdoughs. The interspecies and intraspecies diversity in fermentation performance has been examined in light of interactions with LAB species and strains. Different associations between yeast and LAB strains lead to different acetic acid production levels, revealing the variability of K. humilis strains in their tolerance to acetate (Häggman & Salovaara, 2008a; Häggman & Salovaara, 2008b; Vernocchi et al., 2004). stricter in T. delbrueckii than in S. cerevisiae, delaying CO2 production | from maltose. This reason is why the regular utilization of this species 3.2.2 in the bread industry has not been established. Birch, Petersen, Arneborg, and Hansen (2013) compared the production It is often stated that while known bakery strains of S. cerevisiae Aroma profile complexity of volatile compounds by seven different popular commercial and strains of W. anomalus and T. delbrueckii are able to hydrolyse S. cerevisiae strains. They analysed 52 volatile and aroma compounds maltose, most Kazachstania species are not (Daniel, Moons, Huret, and found that the most powerful odour compounds were 3‐ Vrancken, & De Vuyst, 2011). Indeed, an analysis of Kazachstania type methylbutanal, strains showed that only K. bulderi, Kazachstania piceae, and phenylacetaldehyde. These compounds are formed by a secondary fer- 2,3‐butanedione, 3‐methyl‐1‐butanol, and Kazachstania hellenica are able to degrade maltose. However, recent mentation reaction, the Ehrlich pathway, and contribute to the crumb results suggest that several strains of K. bulderi, K. humilis, K. unispora, aroma (De Vuyst et al., 2016). Differences in aroma compounds were and K. saulgeensis isolated from sourdough are maltose‐positive also linked to fermentation rate (Birch, van den Berg, & Hansen, (Jacques et al., 2016). The molecular mechanisms underlying maltose 2013), and strains with higher growth rates produced a higher concen- utilization by Kazachstania species have not been described yet. The tration of aroma compounds. More recently, Liu et al. (2018) lack of maltose fermentation ability in most Kazachstania type strains compared the aromatic compounds produced in Chinese steamed bread has led to the hypothesis that a noncompetitive interaction with malt- made with six strains of different sourdough yeast species (S. cerevisiae, ose‐positive LAB is compulsory in sourdoughs (De Vuyst, Vrancken, K. humilis, W. anomalus, P. kudriavzevii, and Saccharomycopsis fibuligera). Ravyts, Rimaux, & Weckx, 2009). However, the metabolic diversity They detected 41 aromatic compounds, including 11 alcohols, 11 alde- of both yeast and LAB enables a wide range of different types of inter- hydes, 5 ketones, 9 acids, 3 esters, and 2 other compounds. Most of the actions and associations. These interactions may define the final com- compounds were common among the different breads, but the quantity position of sourdough communities and therefore the characteristics was dependent on the yeast species used. of sourdough bread. Nonconventional yeasts species show high potential for increasing the aroma complexity of bread while insuring fermentation ability 3.2 | Selection of bakery yeast starters (Pacheco et al., 2012). T. delbrueckii and S. bayanus were shown to have appropriate fermentation ability and produce interesting The metabolic and physiological diversity of bakery yeasts offers the aroma profiles; Kluyveromyces marxianus was found to generate bread potential to improve and change the characteristics of the final bread with a more complex aroma profile, a longer shelf‐life, and higher product. S. cerevisiae commercial strains have been artificially selected scores in sensory tests than traditional commercial sourdoughs CARBONETTO 598 ET AL. (Aslankoohi et al., 2016; Plessas, Bekatorou, et al., 2008; Plessas, The type of interaction that yeast and LAB can undergo is deter- Fisher, et al., 2008). More recently, Zhou et al. (2017) showed that mined by the manner in which one species affects the other. The Kazachstania gamospora and Wickerhamomyces subpelliculosus strains effect of species A on species B can be regarded as positive if the pop- presented increased leavening ability relative to a S. cerevisiae com- ulation size of B tends to increase in the presence of A and as negative mercial strain. They also presented a unique aromatic profile and if it decreases. It can also be neutral when the population size of A is higher osmo‐tolerance than S. cerevisiae. unaffected by the presence of B. At least six types of interactions can be detected, namely, (a) a negative/negative interaction described as 3.2.3 | Phytase activity competition for resources; (b) a negative/neutral interaction or Whole grain bread and sourdough bread are gaining popularity due to amensalism; (c) a negative/positive interaction described as predation an increasing awareness of their nutritional benefits. However, whole or parasitism; (d) a positive/neutral interaction called commensalism; grain flour contains considerable amounts of phytic acid, which che- and (e) a positive/positive interaction known as mutualism. Such inter- lates divalent minerals, such as iron and zinc, depleting their bioavail- actions have been documented for yeast and LAB in sourdough com- ability (Sandberg & Svanberg, 1991). It has been shown that the munities. They include competition for resources (competition for phytate content is reduced in sourdough bread (Lopez et al., 2001). glucose, amino acids, etc.), facilitation via cross‐feeding (maltose deg- An analysis of the phytase activity of several sourdough strains has radation by LAB and production of glucose for the microbial commu- revealed variability in the enzymatic activity between species. nity, production of amino acids, etc.), and negative or positive S. cerevisiae exhibited higher activity than K. humilis and P. kudriavzevii interactions via the production of secondary compounds that affect (Nuobariene, Hansen, & Arneborg, 2012; Nuobariene, Hansen, Jesper- the physico‐chemical properties of the environment (antibiotic pro- sen, & Arneborg, 2011; Palla, Cristani, Giovannetti, & Agnolucci, duction, acidification of the environment, toxin killer, etc.). 2017). Enriching the mineral bioavailability of breads through micro- Cross‐feeding involves the utilization of metabolites or waste bial action is an attractive way to enhance the nutritional quality of products of one species as nutrients by a second species (Seth & Taga, 2014). In sourdough, cross‐feeding may happen in both directions. The bread. facilitation of yeasts by LAB can be the result of maltose metabolism. 3.2.4 | Cold tolerance Storage of frozen dough is a common practice in the bakery industry. This process requires cold‐tolerant strains that can retain their fermentative ability after freezing. S. cerevisiae and T. delbrueckii strains isolated from homemade corn and rye bread doughs have shown a higher freezing tolerance than commercial strains while maintaining their leavening capacity (Almeida & Pais, 1996). Comparisons between cold‐tolerant and cold‐sensitive commercial strains have revealed differences in gene expression profiles under stress conditions (Rodriguez‐Vargas, Estruch, & Randez‐Gil, 2002). The main mechanisms in S. cerevisiae include the accumulation of trehalose, glycerol and heat‐shock proteins, and changes in membrane fluidity (Aguilera, Randez‐Gil, & Prieto, 2007). In addition, the stress tolerant phenotype of T. delbrueckii includes lower lipid peroxidation, higher membrane integrity, and higher resistance to H2O2, but no changes in intracellular trehalose concentration (Alvarez‐Perez et al., 2012, Alves‐Araújo, Almeida, Sousa, & Leão, 2004; Pacheco et al., 2012). Extending advances in this field to other yeast species would be very attractive to the commercial baking industry. The lack of maltose fermentation ability in most type strains of Kazachstania sp. has led to the hypothesis that an association with maltose‐positive LAB is favoured by cross‐feeding (De Vuyst & Neysens, 2005; De Vuyst et al., 2009; Gobbetti, 1998; Venturi, Guerrini, & Vincenzini, 2012). One frequently given example is the case of the interaction between K. humilis and L. sanfranciscensis. Maltose‐positive L. sanfranciscensis cells take up maltose from flour and hydrolyse it into glucose and glucose‐1‐phosphate. The latter is further metabolized, whereas the former is released into the environment, preventing high intracellular concentrations. As a consequence, glucose becomes available for fermentation by maltose‐negative K. humilis cells (Gobbetti, 1998; Stolz, Bocker, Vogel, & Hammes, 1993; Venturi et al., 2012). However, some maltose‐positive strains of Kazachstania sp. have been found. Maltose metabolism is not the only explanation for yeast facilitation by LAB. L. sanfranciscensis cells also release amino acids that can be used by yeast cells or other LAB cells (Gobbetti, 1998). In turn, yeast may also facilitate LAB growth through the release of amino acids (Ponomarova et al., 2017), peptides, and vitamins (Frey‐Klett et al., 2011; Gobbetti, 1998; Gobbetti, Corsetti, & Rossi, 1994) or via the hydrolysis of sucrose into glucose and 4 | YEAST/LAB INTERACTIONS IN SO URDO UGH fructose (Gobbetti et al., 1994). During fermentation, yeasts and LAB produce and release other compounds that are not nutrients; instead, these compounds modify A single sourdough usually harbours a few dominant yeast and LAB the physico‐chemical properties of the environment to the advantage species, making it an ideal system for studying the underlying pro- or disadvantage of other species. The lactic acid produced by LAB and cesses of microbial diversity patterns, particularly biotic interactions. the acetic acid produced by LAB and yeast can notably exclude or Here, we present the mechanisms of interactions that have been doc- strongly inhibit the growth of non‐LAB bacterial and fungal contami- umented in the literature regarding microorganisms in sourdough. We nants by decreasing the pH of the environment. This change promotes do not comment on other ecological niches in which LAB and the growth of low‐pH adapted yeasts and LAB strains by reducing the yeast co‐occur (Crowley, Mahony, & van Sinderen, 2013; Frey‐Klett competition that they would have faced from other species. Gänzle, et al., 2011). Ehmann, and Hammes (1998) have found that K. humilis growth was CARBONETTO ET AL. 599 unaffected by pH in the range of 3.5–7. The growth of two strains of Much work remains to be done in order to elucidate the secrets L. sanfranciscensis varied in this range of pH with an optimum at behind the ecology and evolution of yeast in bread. Comprehensive approximately 5.5. However, the growth of both K. humilis and analyses of S. cerevisiae populations isolated from bakery environ- L. sanfranciscensis decreased with increasing concentrations of lactate ments will elucidate domestication, polyploidization, and gene transfer or acetate. events. Genomic and phenomic analysis of Kazachstania bakery spe- LAB species, such as Lactobacillus cies will elucidate species radiation and adaptation processes. More- amylovorus, or L. plantarum, are known to produce antibiotics or pro- over, a deeper characterization of yeast dispersion from hypothetical tein‐based bacteriocins (Crowley et al., 2013; De Vuyst et al., 2009; sources (i.e., flour, water, baker's hands, and air) is pending. Finally, Joerger, 2003). The inhibitory spectrum of these compounds seems interactions between yeast and LAB need further exploration. The to be specifically aimed at cereal‐associated microbiota (Gobbetti, nature of the interactions among most of the described species has 1998). L. sanfranciscensis strain C57 produces a bacteriocin peptide not been well studied yet. The answers to these remaining questions active against almost every other sourdough LAB species and the will shed light on the mechanisms and processes behind microbial pathogenic bacterium Listeria monocytogenes. L. sanfranciscensis strain diversity and could guide new conservation strategies. We think that C51 produces a mixture of organic acids that inhibit most bread spoil- most of these yet‐to‐answer questions will greatly benefit from the age moulds, fungi, and some Candida species. Yeast also produce bac- implementation of participatory research approaches; mainly regard- teriocin‐like toxic compounds, and some strains of S. cerevisiae are ing species sources and interactions. As mentioned, huge efforts are known to produce compounds with antibacterial activities (Al‐Jassani, being conducted by France and the United States teams in order to Mohammed, & Hameed, 2016; Osborne & Edwards, 2007). It is not integrate the study of biological and sociocultural diversity using citi- known whether these compounds are important in the bread and bak- zen science methods. The main goals of these projects are the study ery ecosystem. of microbial diversity and evolution but with a dedicated focus on Lactobacillus reuterii, These facilitation and competition interactions, and others that the collection of cultural and social metadata provided by bakers. As have not yet been described, can impact the composition and struc- a final result, the acquired knowledge will lead to the implementation ture of sourdough microbial communities. As the ability to produce of better policies of conservation for both the biological and cultural some aromas and flavours depends on the microbial species, commu- diversity behind bread. nity composition may influence the volatile compounds found in sourdough and could consequently affect bread flavour. However, the ACKNOWLEDGEMENTS nature of most LAB and yeast associations have not yet been studied, This work was supported by Agence Nationale de la Recherche grant and the relationship between the diversity of compounds and sour- (ANR‐13‐ALID‐0005 BAKERY, France) and a Fonds de dotation EKIP dough community composition is yet to be uncovered. project (France). The author would like to thank Kate Howell for critically reading and commenting on the manuscript as well as all partners of the BAKERY and EKIP project. The authors would like to 5 | C O N CL U S I O N S thank Marc‐André Lachance and two reviewers for critical comments and improvment of the manuscript. Bread is an appealing system to study the ecological and evolutionary processes underlying yeast diversity for several reasons: (a) the history of bread making is well documented, and bread is found worldwide; (b) the bread production process is easily replicable, and dough can be easily sampled; (c) S. cerevisiae is the best known yeast species, making population analysis simpler, and bakery strains vary in ploidy, enabling studies on the incidence and evolution of polyploidy; (d) insights into the population structure of several non‐Saccharomyces bakery yeasts species at the genomic level could easily be obtained and compared as their genomes have been sequenced (W. anomalus, T. delbrueckii, P. kudriavzevii, and K. saulgeensis) or soon will be (K. bulderi and K. humilis); (e) sourdough microbial communities are relatively simple, and sourdough community members are easily isolated and grown in lab conditions; and (f) the replication of sourdough environmental conditions is possible in the laboratory, but sourdough can also be studied in situ in bakeries using a participatory research approach. The fact that sourdoughs can be maintained for years also enables the analysis of microbial populations and community dynamics and evolution. The opportunity to perform an experimental dissection of patterns of diversity in vitro makes bread (particularly sourdough) into a good model for studying microbial evolution in action and the impact of human practices on microbial community assembly. ORCID Belén Carbonetto Thibault Nidelet Judith Legrand Delphine Sicard http://orcid.org/0000-0002-2784-5324 http://orcid.org/0000-0002-0713-7160 http://orcid.org/0000-0001-5157-9268 http://orcid.org/0000-0002-6570-3212 RE FE RE NC ES Aguilera, J., Randez‐Gil, F., & Prieto, J. A. (2007). Cold response in Saccharomyces cerevisiae: New functions for old mechanisms. FEMS Microbiology Reviews, 31, 327–341. Albertin, W., Marullo, P., Aigle, M., Bourgais, A., Bely, M., Dillmann, C., … Sicard, D. (2009). Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: Towards a new domesticated species. Journal of Evolutionary Biology, 22, 2157–2170. Al‐Jassani, M., Mohammed, G., & Hameed, I. (2016). Secondary metabolites analysis of Saccharomyces cerievisiae and evaluation of antibacterial activity. International Journal of Pharmaceutical and Clinical Research, 8, 304–315. Almeida, M. J., & Pais, C. (1996). Leavening ability and freeze tolerance of yeasts isolated from traditional corn and rye bread doughs. Applied and Environmental Microbiology, 62, 4401–4404. Almeida, P., Barbosa, R., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., … Sampaio, J. P. (2015). A population genomics insight into the CARBONETTO 600 Mediterranean origins of wine yeast domestication. Molecular Ecology, 24, 5412–5427. Alvarez‐Perez, S., Mateos, A., Dominguez, L., Martinez‐Nevado, E., Rodriguez‐Bertos, A., Blanco, J. L., & Garcia, M. E. (2012). First isolation of the anamorph of Kazachstania heterogenica from a fatal infection in a primate host. Medical Mycology, 50, 193–196. ET AL. De Vuyst, L., Harth, H., Van Kerrebroeck, S., & Leroy, F. (2016). Yeast diversity of sourdoughs and associated metabolic properties and functionalities. International Journal of Food Microbiology, 239, 26–34. De Vuyst, L., Van Kerrebroeck, S., Harth, H., Huys, G., Daniel, H.‐M., & Weckx, S. (2014). Microbial ecology of sourdough fermentations: Diverse or uniform? Food Microbiology, 37, 11–29. Alves‐Araújo, C., Almeida, M. J., Sousa, M. J., & Leão, C. (2004). Freeze tolerance of the yeast Torulaspora delbrueckii: Cellular and biochemical basis. FEMS Microbiology Letters, 240, 7–14. De Vuyst, L., Van Kerrebroeck, S., & Leroy, F. (2017). Microbial ecology and process technology of sourdough fermentation. Advanced in Applied Microbiology, 100, 49–160. Alves‐Araújo, C., Pacheco, A., Almeida, M. J., Spencer‐Martins, I., Leão, C., & Sousa, M. J. (2007). Sugar utilization patterns and respiro‐fermentative metabolism in the baker's yeast Torulaspora delbrueckii. Microbiology, 153, 898–904. De Vuyst, L., Vrancken, G., Ravyts, F., Rimaux, T., & Weckx, S. (2009). Biodiversity, ecological determinants, and metabolic exploitation of sourdough microbiota. Food Microbiology, 26, 666–675. Araújo, F. V., Rosa, C. A., Freitas, L. F. D., Lachance, M.‐A., Vaughan‐Martini, A., Mendonça‐Hagler, L. C., & Hagler, A. N. (2012). Kazachstania bromeliacearum sp. nov., a yeast species from water tanks of bromeliads. International Journal of Systematic and Evolutionary Microbiology, 62, 1002–1006. Aslankoohi, E., Herrera‐Malaver, B., Rezaei, M. N., Steensels, J., Courtin, C. M., & Verstrepen, K. J. (2016). Non‐conventional yeast strains increase the aroma complexity of bread. PLoS One, 11, e0165126. Bell, P. J., Higgins, V. J., & Attfield, P. V. (2001). Comparison of fermentative capacities of industrial baking and wild‐type yeasts of the species Saccharomyces cerevisiae in different sugar media. Letters in Applied Microbiology, 32, 224–229. Birch, A. N., Petersen, M. A., Arneborg, N., & Hansen, Å. S. (2013). Influence of commercial baker's yeasts on bread aroma profiles. Food Research International, 52, 160–166. Birch, A. N., van den Berg, F. W. J., & Hansen, Å. S. (2013). Expansion profiles of wheat doughs fermented by seven commercial baker's yeasts. Journal of Cereal Science, 58, 318–323. Blandino, A., Al‐Aseeri, M. E., Pandiella, S. S., Cantero, D., & Webb, C. (2003). Cereal‐based fermented foods and beverages. Food Research International, 36, 527–543. Brown, C. A., Murray, A. W., & Verstrepen, K. J. (2010). Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Current Biology, 20, 895–903. Cardinali, G., Antonielli, L., Corte, L., Roscini, L., Bagnetti, A., Pelliccia, C., & Puddu, G. (2012). Kazachstania ichnusensis sp. nov., a diploid homothallic ascomycetous yeast from Sardinian lentisk rhizosphere. International Journal of Systematic and Evolutionary Microbiology, 62, 722–727. Chan, G., Gan, H., Ling, H., & Rashid, N. (2012). Genome sequence of Pichia kudriavzevii M12, a potential producer of bioethanol and phytase. Eukaryotic Cell, 11, 1300–1301. Decimo, M., Quattrini, M., Ricci, G., Fortina, M., & Express, B.‐M. (2017). Evaluation of microbial consortia and chemical changes in spontaneous maize bran fermentation. AMB Express, 7, 205. Delcour, J. A., Bruneel, C., Derde, L. J., Gomand, S. V., Pareyt, B., Putseys, J. A., … Lamberts, L. (2010). Fate of starch in food processing: From raw materials to final food products. Annual Review of Food Science and Technology, 1, 87–111. Desiye, A., & Abegaz, K. (2013). Isolation, characterization and identification of lactic acid bacteria and yeast involved in fermentation of Teff (EragrostisTef) Batter. Advances Research in Biological Sciences, 1, 36–44. Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature, 418, 700. Fay, J. C., & Benavides, J. A. (2005). Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genetics, 1, e5–71. Foschino, R., Gallina, S., Andrighetto, C., Rossetti, L., & Galli, A. (2004). Comparison of cultural methods for the identification and molecular investigation of yeasts from sourdoughs for Italian sweet baked products. FEMS Yeast Research, 4, 609–618. Frey‐Klett, P., Burlinson, P., Deveau, A., Barret, M., Tarkka, M., & Sarniguet, A. (2011). Bacterial‐fungal interactions: Hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiology and Molecular Biology Reviews, 75, 583–609. Gabriel, V., Lefebvre, D., Vayssier, Y., & Faucher, C. (1999). Characterization of microflora from natural sourdoughs. Microbiologie, Aliments Nutrition, 17, 171–179. Gallone, B., Steensels, J., Prahl, T., Soriaga, L., Saels, V., Herrera‐Malaver, B., … Verstrepen, K. J. (2016). Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell, 166, 1397–1410.e16. Gancedo, J. M. (1998). Yeast carbon catabolite repression. Microbiology and Molecular Biology Reviews, 62, 334–361. Charron, M. J., Read, E., Haut, S. R., & Michels, C. A. (1989). Molecular evolution of the telomere‐associated MAL loci of Saccharomyces. Genetics, 122, 307–316. Gänzle, M. G., Ehmann, M., & Hammes, W. P. (1998). Modeling of growth of Lactobacillus sanfranciscensis and Candida milleri in response to process parameters of sourdough fermentation. Applied and Environmental Microbiology, 64, 2616–2623. Chen, R., Wei, S.‐C., Jiang, Y.‐M., Wang, Q.‐M., & Bai, F.‐Y. (2010). Kazachstania taianensis sp. nov., a novel ascomycetous yeast species from orchard soil. International Journal of Systematic and Evolutionary Microbiology, 60, 1473–1476. Garofalo, C., Silvestri, G., Aquilanti, L., & Clementi, F. (2008). PCR‐DGGE analysis of lactic acid bacteria and yeast dynamics during the production processes of three varieties of Panettone. Journal of Applied Microbiology, 105, 243–254. Corsetti, A., Lavermicocca, P., Morea, M., Baruzzi, F., Tosti, N., & Gobbetti, M. (2001). Phenotypic and molecular identification and clustering of lactic acid bacteria and yeasts from wheat (species Triticum durum and Triticum aestivum) sourdoughs of Southern Italy. International Journal of Food Microbiology, 64, 95–104. Gatto, V., & Torriani, S. (2004). Microbial population changes during sourdough fermentation monitored by DGGE analysis of 16S and 26S rRNA gene fragments. Annals of Microbiology, 54, 31–42. Crowley, S., Mahony, J., & van Sinderen, D. (2013). Current perspectives on antifungal lactic acid bacteria as natural bio‐preservatives. Trends in Food Science & Technology, 33, 93–109. Gibbons, J., & Rinker, D. C. (2015). The genomics of microbial domestication in the fermented food environment. Current Opinion in Genetics & Development, 35, 1–8. Daniel, H.‐M., Moons, M.‐C., Huret, S., Vrancken, G., & De Vuyst, L. (2011). Wickerhamomyces anomalus in the sourdough microbial ecosystem. Antonie Van Leeuwenhoek, 99, 63–73. Gobbetti, M. (1998). The sourdough microflora: Interactions of lactic acid bacteria and yeasts. Trends in Food Science & Technology, 9, 267–274. De Vuyst, D. L., & Neysens, P. (2005). The sourdough microflora: Biodiversity and metabolic interactions. Trends in Food Science and Technology, 16, 43–56. Gélinas, P. (2010). Mapping early patents on baker's yeast manufacture. Comprehensive Reviews in Food Science and Food Safety, 9, 483–497. Gobbetti, M., Corsetti, A., & Rossi, J. (1994). The sourdough microflora. Interactions between lactic acid bacteria and yeasts: Metabolism of amino acids. World Journal of Microbiology and Biotechnology, 10, 275–279. CARBONETTO ET AL. 601 Goddard, M. R., & Greig, D. (2015). Saccharomyces cerevisiae: A nomadic yeast with no niche? FEMS Yeast Research, 15. Kurtzman, C., Fell, J., & Boekhout, T. (2011). The yeasts—A taxonomic study (5th ed.). Elsevier Science. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., … Oliver, S. G. (1996). Life with 6000 genes. Science, 274, 546–567. Kurtzman, C., & Robnett, C. J. (2003). Phylogenetic relationships among yeasts of the'Saccharomyces complex'determined from multigene sequence analyses. FEMS Yeast Research, 3, 417–432. Gomez‐Angulo, J., Vega‐Alvarado, L., Escalante‐García, Z., Grande, R., Gschaedler‐Mathis, A., Amaya‐Delgado, L., … Sanchez‐Flores, A. (2015). Genome sequence of Torulaspora delbrueckii NRRL Y‐50541, isolated from mezcal fermentation. Genome Announcements, 3. Gonçalves, M., Pontes, A., Almeida, P., Barbosa, R., Serra, M., Libkind, D., … Sampaio, J. P. (2016). Distinct domestication trajectories in top‐ fermenting beer yeasts and wine yeasts. Current Biology, 26, 2750–2761. Gordon, J. L., Armisén, D., Proux‐Wéra, E., ÓhÉigeartaigh, S. S., Byrne, K. P., & Wolfe, K. H. (2011). Evolutionary erosion of yeast sex chromosomes by mating‐type switching accidents. PNAS, 108, 20024–20029. Häggman, M., & Salovaara, H. (2008a). Effect of fermentation rate on endogenous leavening of Candida milleri in sour rye dough. Food Research International, 41, 266–273. Häggman, M., & Salovaara, H. (2008b). Microbial re‐inoculation reveals differences in the leavening power of sourdough yeast strains. LWT ‐ Food Science and Technology, 41, 148–154. Hagman, A., Säll, T., Compagno, C., & Piskur, J. (2013). Yeast “make‐accumulate‐consume” life strategy evolved as a multi‐step process that predates the whole genome duplication. PLoS One, 8, e68734. Hammes, W., & Gänzle, M. (1997). Sourdough breads and related products. Microbiology of Fermented Foods, 199–216. Hansen, A., & Schieberle, P. (2005). Generation of aroma compounds during sourdough fermentation: Applied and fundamental aspects. Trends in Food Science and Technology, 16, 85–94. Higgins, V. J., Braidwood, M., Bell, P., Bissinger, P., Dawes, I. W., & Attfield, P. V. (1999). Genetic evidence that high noninduced maltase and maltose permease activities, governed by MALx3‐encoded transcriptional regulators, determine efficiency of gas production by baker's yeast in unsugared dough. Applied and Environmental Microbiology, 65, 680–685. Infantes, M., & Schmidt, J. (1992). Characterization of the yeast flora of natural sourdoughs located in various French areas. Sciences des Aliments. Jacques, N., Sarilar, V., Urien, C., Lopes, M. R., Morais, C. G., Uetanabaro, A. P., … Casaregola, S. (2016). Three novel ascomycetous yeast species of the Kazachstania clade, Kazachstania saulgeensis sp. nov., Kazachstania serrabonitensis sp. nov. and Kazachstania australis sp. nov. Reassignment of Candida humilis to Kazachstania humilis f.a. comb. nov. and Candida pseudohumilis to Kazachstania pseudohumilis f.a. comb. nov. International Journal of Systematic and Evolutionary Microbiology, 66, 5192–5200. James, S. A., Carvajal Barriga, E. J., Portero Barahona, P., Nueno‐Palop, C., Cross, K., Bond, C. J., & Roberts, I. N. (2015). Kazachstania yasuniensis sp. nov., an ascomycetous yeast species found in mainland Ecuador and on the Galápagos. International Journal of Systematic and Evolutionary Microbiology, 65, 1304–1309. Joerger, R. D. (2003). Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poultry Science, 82, 640–647. Kurtzman, C. P., & Robnett, C. J. (1998). Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek, 73, 331–371. Kurtzman, C. P., Robnett, C. J., Ward, J. M., Brayton, C., Gorelick, P., & Walsh, T. J. (2005). Multigene phylogenetic analysis of pathogenic candida species in the Kazachstania (Arxiozyma) telluris complex and description of their ascosporic states as Kazachstania bovina sp. nov., K. heterogenica sp. nov., K. pintolopesii sp. nov., and K. slooffiae sp. nov. Journal of Clinical Microbiology, 43, 101–111. Lacumin, L., Cecchini, F., Manzano, M., Osualdini, M., Boscolo, D., Orlic, S., & Comi, G. (2009). Description of the microflora of sourdoughs by culture‐dependent and culture‐independent methods. Food Microbiology, 26, 128–135. Lattanzi, A., Minervini, F., Cagno, D., Diviccaro, A., Antonielli, L., Cardinali, G., … Gobbetti, M. (2013). The lactic acid bacteria and yeast microbiota of eighteen sourdoughs used for the manufacture of traditional Italian sweet leavened baked goods. International Journal of Food Microbiology, 163, 71–79. Lee, C.‐F., Yao, C.‐H., Liu, Y.‐R., Young, S.‐S., & Chang, K.‐S. (2009). Kazachstania wufongensis sp. nov., an ascosporogenous yeast isolated from soil in Taiwan. Antonie Van Leeuwenhoek, 95, 335–341. Legras, J. L., Galeote, V., Bigey, F., Camarasa, C., Marsit, S., Nidelet, T., … Dequin, S. (2018). Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Molecular Biology and Evolution, 19, 764–778. https:// doi.org/10.1111/mpp.12561 Legras, J.‐L., Merdinoglu, D., Cornuet, J.‐M., & Karst, F. (2007). Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Molecular Ecology, 16, 2091–2102. Lhomme, E., Lattanzi, A., Dousset, X., Minervini, F., De Angelis, M., Lacaze, G., … Gobbetti, M. (2015). Lactic acid bacterium and yeast microbiotas of sixteen French traditional sourdoughs. International Journal of Food Microbiology, 215, 161–170. Lhomme, E., Urien, C., Legrand, J., Dousset, X., Onno, B., & Sicard, D. (2016). Sourdough microbial community dynamics: An analysis during French organic bread‐making processes. Food Microbiology, 53, 41–50. Libkind, D., Hittinger, C. T., Valério, E., Gonçalves, C., Dover, J., Johnston, M., … Sampaio, J. P. (2011). Microbe domestication and the identification of the wild genetic stock of lager‐brewing yeast. PNAS, 108, 14539–14544. Limtong, S., Yongmanitchai, W., Tun, M. M., Kawasaki, H., & Seki, T. (2007). Kazachstania siamensis sp. nov., an ascomycetous yeast species from forest soil in Thailand. International Journal of Systematic and Evolutionary Microbiology, 57, 419–422. Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., … Louis, E. J. (2009). Population genomics of domestic and wild yeasts. Nature, 458, 337–341. Jouhten, P., Ponomarova, O., Gonzalez, R., & Patil, K. R. (2016). Saccharomyces cerevisiae metabolism in ecological context. FEMS Yeast Research, 16, 1–7. Liu, T., Li, Y., Sadiq, F. A., Yang, H., Gu, J., Yuan, L., … He, G. (2018). Predominant yeasts in Chinese traditional sourdough and their influence on aroma formation in Chinese steamed bread. Food Chemistry, 242, 404–411. Kabisch, J., Erl‐Höning, C., Wenning, M., Böhnlein, C., Gareis, M., & Pichner, R. (2016). Spoilage of vacuum‐packed beef by the yeast Kazachstania psychrophila. Food Microbiology, 53, 15–23. Lombardi, Zilio, F., Andrighetto, C., Zampese, L., & Loddo, A. Microbiological characterization of sourdoughs of Veneto region. Industrie Alimentari. Kabisch, J., Höning, C., Böhnlein, C., Pichner, R., Gareis, M., & Wenning, M. (2013). Kazachstania psychrophila sp. nov., a novel psychrophilic yeast isolated from vacuum‐packed beef. Antonie Van Leeuwenhoek, 104, 925–931. Lopez, H. W., Krespine, V., Guy, C., Messager, A., Demigne, C., & Remesy, C. (2001). Prolonged fermentation of whole wheat sourdough reduces phytate level and increases soluble magnesium. Journal of Agricultural and Food Chemistry, 49, 2657–2662. Kim, S., Kim, J., Yun, E., & Kim, K. (2016). Food metabolomics: From farm to human. Current Opinion in Biotechnology, 37, 16–23. Lu, H.‐Z., Cai, Y., Wu, Z.‐W., Jia, J.‐H., & Bai, F.‐Y. (2004). Kazachstania aerobia sp. nov., an ascomycetous yeast species from aerobically CARBONETTO 602 deteriorating corn silage. International Journal of Systematic and Evolutionary Microbiology, 54, 2431–2435. Ludlow, C. L., Cromie, G. A., Cecilia, G.‐T., Sirr, A., Hays, M., Field, C., … Dudley, A. M. (2016). Independent origins of yeast associated with coffee and cacao fermentation. Current Biology, 26, 965–971. Mäntynen, V. H., Korhola, M., Gudmundsson, H., Turakainen, H., Alfredsson, G. A., Salovaara, H., & LindstrÖm, K. (1999). A polyphasic study on the taxonomic position of industrial sour dough yeasts. Systematic and Applied Microbiology, 22, 87–96. McGovern, P. (2009). Uncorking the past: The quest for wine, beer, and other alcoholic beverages. McGovern, P. (2013). Ancient wine: The search for the origins of viniculture. Meroth, C. B., Hammes, W. P., & Hertel, C. (2003). Identification and population dynamics of yeasts in sourdough fermentation processes by PCR‐denaturing gradient gel electrophoresis. Applied and Environmental Microbiology, 69, 7453–7461. Minervini, F., Lattanzi, A., De Angelis, M., Celano, G., & Gobbetti, M. (2015). House microbiotas as sources of lactic acid bacteria and yeasts in traditional Italian sourdoughs. Food Microbiology, 52, 66–76. Minervini, F., Cagno, R. D., Lattanzi, A., Angelis, M. D., Antonielli, L., Cardinali, G., … Gobbetti, M. (2012). Lactic acid bacterium and yeast microbiotas of 19 sourdoughs used for traditional/typical Italian breads: Interactions between ingredients and microbial species diversity. Applied and Environmental Microbiology, 78, 1251–1264. Minervini, F., Lattanzi, A., De Angelis, M., Di Cagno, R., & Gobbetti, M. (2012). Influence of Artisan bakery‐ or laboratory‐propagated sourdoughs on the diversity of lactic acid bacterium and yeast microbiotas. Applied and Environmental Microbiology, 78, 5328–5340. https://doi.org/10.1128/AEM.00572‐12 Mondal, A., & Datta, A. K. (2008). Bread Baking—A Review., 86, 465–474. Naumov, G. I., Naumova, E. S., & Michels, C. A. (1994). Genetic variation of the repeated MAL loci in natural populations of Saccharomyces cerevisiae and Saccharomyces paradoxus. Genetics, 136, 803–812. Needleman, R. (1991). Control of maltase synthesis in yeast. Molecular Microbiology, 5, 2079–2084. Needleman, R. B., Kaback, D. B., Dubin, R. A., Perkins, E. L., Rosenberg, N. G., Sutherland, K. A., … Michels, C. A. (1984). MAL6 of Saccharomyces: A complex genetic locus containing three genes required for maltose fermentation. Proceedings of the National Academy of Sciences of the United States of America, 81, 2811–2815. Nisiotou, A. A., & Nychas, G.‐J. E. (2008). Kazachstania hellenica sp. nov., a novel ascomycetous yeast from a Botrytis‐affected grape must fermentation. International Journal of Systematic and Evolutionary Microbiology, 58, 1263–1267. Nuobariene, L., Hansen, Å. S., & Arneborg, N. (2012). Isolation and identification of phytase‐active yeasts from sourdoughs. LWT ‐ Food Science and Technology, 48, 190–196. Nuobariene, L., Hansen, A. S., Jespersen, L., & Arneborg, N. (2011). Phytase‐active yeasts from grain‐based food and beer. Journal of Applied Microbiology, 110, 1370–1380. Obiri‐Danso, K. (1994). Microbiological studies on corn dough fermentation. Cereal Chemistry, 71, 186–188. Oda, Y., & Ouchi, K. (1989). Principal‐component analysis of the characteristics desirable in baker's yeasts. Applied and Environmental Microbiology, 55, 1495–1499. Osborne, J. P., & Edwards, C. G. (2007). Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. International Journal of Food Microbiology, 118, 27–34. Osimani, A., Zannini, E., Aquilanti, L., Mannazzu, I. M., Comitini, F., & Clementi, F. (2009). Lactic acid bacteria and yeasts from wheat sourdoughs of the Marche region. Italian Journal of Food Science, 21, 269–286. ET AL. Pacheco, A., Santos, J., Chaves, S., Almeida, J., Leão, C., & Sousa, M. J. (2012). The emerging role of the yeast Torulaspora delbrueckii in bread and wine production: Using genetic manipulation to study molecular basis of physiological responses. Structure and Function of Food Engineering. Palla, M., Cristani, C., Giovannetti, M., & Agnolucci, M. (2017). Identification and characterization of lactic acid bacteria and yeasts of PDO Tuscan bread sourdough by culture dependent and independent methods. International Journal of Food Microbiology, 250, 19–26. Park, H., Ko, H., Jeong, H., Lee, S., Ko, H. J., Bae, J. H., … Sohn, J. H. (2018). Draft genome sequence of a multistress‐tolerant yeast, Pichia kudriavzevii NG7. Genome Announcements, 6(3), pii: e01515‐17. Peter, J., De Chiara, M., Friedrich, A., Yue, J.‐X., Pflieger, D., Bergström, A., et al. (2018). Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature, 556, 339–344. Plessas, S., Bekatorou, A., Gallanagh, J., Nigam, P., Koutinas, A. A., & Psarianos, C. (2008). Evolution of aroma volatiles during storage of sourdough breads made by mixed cultures of Kluyveromyces marxianus and Lactobacillus delbrueckii ssp. bulgaricus or Lactobacillus helveticus. Food Chemistry, 107, 883–889. Plessas, S., Fisher, A., Koureta, K., Psarianos, C., Nigam, P., & Koutinas, A. A. (2008). Application of Kluyveromyces marxianus, Lactobacillus delbrueckii ssp. bulgaricus and L. helveticus for sourdough bread making. Food Chemistry, 106, 985–990. Ponomarova, O., Gabrielli, N., Sévin, D. C., Mülleder, M., Zirngibl, K., Bulyha, K., … Patil, K. R. (2017). Yeast creates a niche for symbiotic lactic acid bacteria through nitrogen overflow. Cell Systems, 5, 345–357.e6. Pulvirenti, A., Caggia, C., Restuccia, C., Gullo, M., & Giudici, P. (2001). DNA fingerprinting methods used for identification of yeasts isolated from Sicilian sourdoughs. Annals of Microbiology. Randez‐Gil, F., Córcoles‐Sáez, I., & Prieto, J. A. (2013). Genetic and phenotypic characteristics of baker's yeast: Relevance to baking. Annual Review of Food Science and Technology, 4, 191–214. Riley, R., Haridas, S., Wolfe, K. H., Lopes, M. R., Hittinger, C. T., Göker, M., … Jeffries, T. W. (2016). Comparative genomics of biotechnologically important yeasts. PNAS, 113, 9882–9887. Rodriguez‐Vargas, S., Estruch, F., & Randez‐Gil, F. (2002). Gene expression analysis of cold and freeze stress in baker's yeast. Applied and Environmental Microbiology, 68, 3024–3030. Roussel, P., & Chiron, H. (2005). Les pains français (2nd ed.). https://www. lavoisier.fr/livre/agro-alimentaire/les‐pains‐francais‐evolution‐qualite‐ production‐2‐ed/roussel/descriptif_2261627 Saeed, M., Anjum, F., Zahoor, T., Nawaz, H., & Sajjad‐Ur‐Rehman (2009). Isolation and characterization of starter culture from spontaneous fermentation of sourdough. International Journal of Agriculture and Biology. Safar, S. V. B., Gomes, F. C. O., Marques, A. R., Lachance, M.‐A., & Rosa, C. A. (2013). Kazachstania rupicola sp. nov., a yeast species isolated from water tanks of a bromeliad in Brazil. International Journal of Systematic and Evolutionary Microbiology, 63, 1165–1168. Salovaara, H., & Savolainen, J. (1984). Yeast type isolated from Finnish sour rye dough starters. Polonica: Acta Aliment. Salque, M., Bogucki, P. I., Pyzel, J., Sobkowiak‐Tabaka, I., Grygiel, R., Szmyt, M., & Evershed, R. P. (2013). Earliest evidence for cheese making in the sixth millennium in northern Europe. Nature, 493, 522–525. Samuel, D. (1994). An archaeological study of baking and bread in New Kingdom Egypt. Samuel, D. (1996). Investigation of ancient Egyptian baking and brewing methods by correlative microscopy. Science, 273, 488–490. Samuel, D. (2002). Bread in archaeology. Civilisations. Revue Internationale d'anthropologie et de Sciences Humaines, 27–36. Sandberg, A.‐S., & Svanberg, U. (1991). Phytate hydrolysis by phytase in cereals; effects on in vitro estimation of iron availability. Journal of Food Science, 56, 1330–1333. Sarilar, V., Sterck, L., Matsumoto, S., Jacques, N., Neuvéglise, C., Tinsley, C. R., … Casaregola, S. (2017). Genome sequence of the type strain CLIB CARBONETTO ET AL. 1764 T (=CBS 14374 T) of the yeast species Kazachstania saulgeensis isolated from French organic sourdough. Genom Data, 13, 41–43. Schacherer, J., Shapiro, J. A., Ruderfer, D. M., & Kruglyak, L. (2009). Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature, 458, 342–345. Scheirlinck, I., Van der Meulen, R., Van Schoor, A., Vancanneyt, M., De Vuyst, L., Vandamme, P., & Huys, G. (2007). Influence of geographical origin and flour type on diversity of lactic acid bacteria in traditional Belgian sourdoughs. Applied and Environmental Microbiology, 73, 6262–6269. Seth, E. C., & Taga, M. E. (2014). Nutrient cross‐feeding in the microbial world. Frontiers in Microbiology, 5, 350. Shevchenko, A., Yang, Y., Knaust, A., Thomas, H., Jiang, H., Lu, E., … Shevchenko, A. (2014). Proteomics identifies the composition and manufacturing recipe of the 2500‐year old sourdough bread from Subeixi cemetery in China. Journal of Proteomics, 105, 363–371. Sicard, D., & Legras, J.‐L. (2011). Bread, beer and wine: Yeast domestication in the Saccharomyces sensu stricto complex. Comptes Rendus Biologies, 334, 229–236. Spicher, G., & Schröder, R. (1978). Die Mikroflora des Sauerteiges. IV. Mitteilung: Untersuchungen über die Art der in “Reinzuchtsauern” anzutreffenden stäbchenförmigen Milchsäurebakterien (Genus Lactobacillus Beijerinck). Zeitschrift für Lebensmittel‐Untersuchung und ‐ Forschung, 167, 342–354. 603 Vigentini, I., Antoniani, D., Roscini, L., Comasio, A., Galafassi, S., Picozzi, C., … Foschino, R. (2014). Candida milleri species reveals intraspecific genetic and metabolic polymorphisms. Food Microbiology, 42, 72–81. Vogel, R. F., Mueller, M., Stolz, P., & Ehrmann, M. (1996). Ecology in sourdoughs produced by traditional and modern technologies. Advances in Food Sciences, 18, 152–159. Voordeckers, K., Brown, C., Voordeckers, C., Brown, C. A., Vanneste, K., van der Zande, E., … Verstrepen, K. J. (2012). Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biology, 10, e1001446. Vrancken, G., De Vuyst, L., Van der Meulen, R., Huys, G., Vandamme, P., & Daniel, H.‐M. (2010). Yeast species composition differs between artisan bakery and spontaneous laboratory sourdoughs. FEMS Yeast Research, 10, 471–481. Warringer, J., Zörgö, E., Cubillos, F. A., Zia, A., Gjuvsland, A., Simpson, J. T., … Blomberg, A. (2011). Trait variation in yeast is defined by population history. PLoS Genetics, 7, e1002111. Wolfe, K. H., Armisén, D., Proux‐Wera, E., ÓhÉigeartaigh, S. S., Azam, H., Gordon, J. L., & Byrne, K. P. (2015). Clade‐ and species‐specific features of genome evolution in the Saccharomycetaceae. FEMS Yeast Research, 15, fov035. Wu, B., Buljic, A., & Hao, W. (2015). Extensive horizontal transfer and homologous recombination generate highly chimeric mitochondrial genomes in yeast. Molecular Biology and Evolution, 32, 2559–2570. Steensels, J., Snoek, T., Meersman, E., Nicolino, M. P., Voordeckers, K., & Verstrepen, K. J. (2014). Improving industrial yeast strains: Exploiting natural and artificial diversity. FEMS Microbiology Reviews, 38, 947–995. Wu, Z.‐W., & Bai, F.‐Y. (2005). Kazachstania aquatica sp. nov. and Kazachstania solicola sp. nov., novel ascomycetous yeast species. International Journal of Systematic and Evolutionary Microbiology, 55, 2219–2224. Succi, M., Reale, A., Andrighetto, C., Lombardi, A., Sorrentino, E., & Coppola, R. (2003). Presence of yeasts in southern Italian sourdoughs from Triticum aestivum flour. FEMS Microbiology Letters, 225, 143–148. Zhang, G., Sadiq, F. A., Zhu, L., Liu, T., Yang, H., Wang, X., & He, G. (2015). Investigation of microbial communities of Chinese sourdoughs using culture‐dependent and DGGE approaches. Journal of Food Science, 80, M2535–M2542. Stolz, P., Bocker, G., Vogel, R. F., & Hammes, W. P. (1993). Utilisation of maltose and glucose by lactobacilli isolated from sourdough. FEMS Microbiology Reviews, 109, 237–242. Sugihara, T., Kline, L., & Miller, M. (1971). Microorganisms of the San Francisco sour dough bread process I. Yeasts Responsible for the Leavening Action. Applied Microbiology, 21, 456–458. Suh, S.‐O., & Zhou, J. J. (2011). Kazachstania intestinalis sp. nov., an ascosporogenous yeast from the gut of passalid beetle Odontotaenius disjunctus. Antonie Van Leeuwenhoek, 100, 109–115. Valmorri, S., Tofalo, R., Settanni, L., Corsetti, A., & Suzzi, G. (2010). Yeast microbiota associated with spontaneous sourdough fermentations in the production of traditional wheat sourdough breads of the Abruzzo region (Italy). Antonie Van Leeuwenhoek, 97, 119–129. Venturi, M., Guerrini, S., & Vincenzini, M. (2012). Stable and non‐competitive association of Saccharomyces cerevisiae, Candida milleri and Lactobacillus sanfranciscensis during manufacture of two traditional sourdough baked goods. Food Microbiology, 31, 107–115. Vernocchi, P., Valmorri, S., Gatto, V., Torriani, S., Gianotti, A., Suzzi, G., … Gardini, F. (2004). A survey on yeast microbiota associated with an Italian traditional sweet‐leavened baked good fermentation. Food Research International, 37, 469–476. Zhang, J., Liu, W., Sun, Z., Bao, Q., Wang, F., Yu, J., … Zhang, H. (2011). Diversity of lactic acid bacteria and yeasts in traditional sourdoughs collected from western region in Inner Mongolia of China. Food Control, 22, 767–774. Zhou, N., Schifferdecker, A. J., Gamero, A., Compagno, C., Boekhout, T., Piškur, J., & Knecht, W. (2017). Kazachstania gamospora and Wickerhamomyces subpelliculosus: Two alternative baker's yeasts in the modern bakery. International Journal of Food Microbiology, 250, 45–58. SUPPORTI NG INFORMATION Additional supporting information may be found online in the Supporting Information section at the end of the article. How to cite this article: Carbonetto B, Ramsayer J, Nidelet T, Legrand J, Sicard D. Bakery yeasts, a new model for studies in ecology and evolution. Yeast. 2018;35:591–603. https://doi. org/10.1002/yea.3350