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Nidelet, T.

Publications and source records attributed to Nidelet, T..

10 recordsLinked to original sources

Genotypic and phenotypic diversity of Maudiozyma humilis: the multiple evolutionary trajectories of a domesticated yeast

Maudiozyma humilis is the second most frequently encountered yeast species in sourdough bread. Despite its ecological and food relevance, little is known about its evolutionary trajectories and phenotype traits of interest. Here we investigated the genomic and phenotypic diversity of a world-wide collection of 55 M. humilis strains, including 52 from sourdough, by combining genomic analysis, flow cytometry and high-throughput phenotyping of fermentation kinetics and fitness. Population genomic analysis revealed six genetically distinct clades, three diploid and three triploid, with no geographical or substrate-specific structuring. Phylogenetic, loss of heterozygosity (LOH) distribution and allele specific analysis indicated that triploid strains originated from both recent and more ancient hybridization events involving multiple diploid lineages. The absence of the HO gene, and mating-type silent cassettes, revealed that M. humilis is not able to carry mating-type switching. In addition, high linkage disequilibrium (LD) and variable LOH accumulation were observed consistent with a predominantly clonal reproduction. Last, an exceptionally high level of heterozygosity was detected, suggesting that occasional hybridization is the major driver of genetic diversity. Phenotypic characterization in a synthetic sourdough medium revealed variation in fermentation kinetics and fitness statistically associated with the genetic clades. Interestingly, genetic distance between clades and strains better explain the phenotypic variation than difference in ploidy. Altogether, our findings highlight the complex evolutionary history of M. humilis, shaped by hybridization and ploidy variation and reveal that historical contingency, more than ploidy, shapes the phenotypic landscape of this species. Beyond providing the first analysis of M. humilis evolution, our result challenges the hypothesis that increases in ploidy are necessarily beneficial in domesticated species.

genomics↗

Environmental complexity constrains evolutionary adaptation across taxa

Complex environments combining multiple stressors are the new norm worldwide. Adaptive evolution will be critical to population persistence under these combined challenges, but how environmental complexity affects the pace of evolution remains poorly understood. Using a meta-experimental evolution approach, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors and their pairwise combinations for multiple generations, while keeping the overall stress level comparable. Populations evolving under combined stressors tended to have lower fitness increase in the selective environments, higher fitness reductions in the control environment, and shallower relation between initial maladaptation and fitness gain, than under single stressors. However, these responses varied with species and stressor type. Accounting for such constraints on evolutionary dynamics should prove crucial for the management of biodiversity. Significance StatementA pressing challenges for modern science and society in the face of ongoing global change is understanding what limits the capacity of living organisms to adapt to complex environments combining multiple stressors. To answer to this question, we conducted a large-scale meta-experimental evolution design across a diversity of organisms, exposing them for multiple generations to either single or combined-stress treatments. Combined stressors led to less adaptive fitness gain than single stressors, and imposed additional costs through reduced fitness in non-stressful conditions. This unique combination of meta-experimental approach with a careful distinction between environmental complexity and overall stress allowed us to gain robust quantitative evidence on how environmental complexity can impact the pace of evolution.

evolutionary biology↗

S. cerevisiae serves as keystone species for spoilage resistance in experimental synthetic wine yeast communities

Species diversity is a commonly stated contributor to the fate of an invader, and thus community resistance, in both microbial and non-microbial communities. Termed the "diversity-invasion hypothesis", a positive relationship between diversity and resistance to invasion is observed when an introduced species exhibits lower levels of survival in resident communities with higher species richness. The diversity-invasion hypothesis is an attractive perspective with convincing theory and examples, yet an "invasion paradox" of contrasting results means that a positive role of diversity against invasion is still not a certainty and under debate. In this study we investigated the relationship between resistance to invasion and resident community species richness versus species identity (i.e., keystone species). Using synthetic communities comprised of combinations of four wine yeasts (Saccharomyces cerevisiae, Lachancea thermotolerans, Torulaspora delbrueckii, Starmerella bacillaris), we tracked over 21 days the presence of introduced Brettanomyces bruxellensis spoilage yeast and Lactiplantibacillus plantarum lactic acid bacteria to ask the following: 1. Does yeast community species richness impact the establishment of B. bruxellensis yeast and L. plantarum bacteria during wine fermentation? 2. How does yeast species identity influence such establishment? We found that species identity rather than richness drove the prevention of establishment of B. bruxellensis and L. plantarum, with S. cerevisiae playing a critical keystone species role. Aside from spoilage prevention by S. cerevisiae, the four resident yeast species demonstrated a strict dominance ranking of competitive exclusion regardless of background community composition. Our research lends evidence against the commonly predicted positive relationship between species richness and resistance to invasion. Furthermore, as spontaneously fermented natural wines and diverse starter cultures gain popularity, our findings support a remaining importance of S. cerevisiae in preventing B. bruxellensis spoilage..

ecology↗

Design of a new model yeast consortium for ecological studies of enological fermentation

Wine fermentation involves complex microbial communities of non-Saccharomyces yeast species besides the well-known Saccharomyces cerevisiae. While extensive research has enhanced our understanding of S. cerevisiae, the development of multi-species fermentation starters has led to increased interest in yeast interactions and the role of microbial diversity in winemaking. Consequently, molecular methods have emerged to identify the different species at different stages of the winemaking process. Model microbial communities or consortia, which provide simplified systems resembling natural microbial diversity, offer opportunities to investigate population dynamics and understand the role of community diversity in ecosystem performance. Here, this work aims to design a yeast consortium reflecting the diversity of wine yeasts and to develop a method for accurately tracking their population dynamics during fermentation. We developed and characterized a six-species consortium, with S. cerevisiae, Hanseniaspora uvarum, Starmerella bacillaris, Metschnikowia pulcherrima, Lachancea thermotolerans and Torulaspora delbrueckii. By tagging each yeast species with distinct fluorescent markers, the study enables real-time monitoring of individual species within the consortium using flow cytometry. We have carried out a complete analysis of this consortium, studying the evolution of populations over time and examining factors such as metabolite production and fermentation kinetics. In addition, the yeast consortium was used to test the diversity-function relationship as a proof of concept. We sought to determine the impact of the initial evenness on communities performances subjected to osmotic stress. To this end, ten randomly designed consortia with varying initial species proportions were followed in enological fermentation with 200 and 280 g/L of initial sugars. The initial proportion of certain species affected the population dynamics and metabolite production however no demonstrable effect of the initial evenness on the response to osmotic stress was shown. These results demonstrated the usefulness of the presented consortium, which is now available to the scientific community and can contribute to future work trying to decipher multispecies dynamics and the role of yeast diversity in wine fermentation.

microbiology↗

Phenotypic variations of primary metabolites yield during alcoholic fermentation in the Saccharomyces cerevisiae species

Saccharomyces cerevisiae is a major actor in winemaking that converts sugars from the grape must into ethanol and CO2 with outstanding efficiency. Primary metabolites produced during fermentation have a great importance in wine. While ethanol content contributes to the overall profile, other metabolites like glycerol, succinate, etc., also have significant impacts, even when present in lower concentrations. S. cerevisiae is known for its great genetic diversity that is related to its natural or technological environment. However, its range of metabolic diversity which can be exploited to enhance wine quality depends on the pathway considered. Our experiment assessed the diversity of primary metabolites production in a set of 51 S. cerevisiae strains from various genetic backgrounds. Results pointed out great yield differences depending on the metabolite considered, with ethanol having the least variation. A negative correlation between ethanol and glycerol was observed, confirming glycerol synthesis as a suitable lever to reduce ethanol yield. Genetic groups were linked to specific metabolic yields such as -ketoglutarate or acetate. This research highlights the potential of using natural yeast diversity in winemaking and provides detailed data set on metabolite production of well known (ethanol, glycerol, acetate) or little-known (lactate) primary metabolites production.

microbiology↗

Data integration uncovers the metabolic bases of phenotypic variation in yeast

The relationship between different levels of integration is a key feature for understanding the genotype-phenotype map.Here, we describe a novel method of integrated data analysis that incorporates protein abundance data into constraint-based modeling to elucidate the biological mechanisms underlying phenotypic variation. Specifically, we studied yeast genetic diversity at three levels of phenotypic complexity in a population of yeast obtained by pairwise crosses of eleven strains belonging to two species, Saccha-romyces cerevisiae and S. uvarum. The data included protein abundances, integrated traits (life-history/fermentation) and computational estimates of metabolic fluxes.Results highlighted that the negative correlation between production traits such as population carrying capacity (K) and traits associated with growth and fermentation rates (Jmax) is explained by a differential usage of energy production pathways: a high K was associated with high TCA fluxes, while a high Jmax was associated with high glycolytic fluxes. Enrichment analysis of protein sets confirmed our results.This powerful approach allowed us to identify the molecular and metabolic bases of integrated trait variation, and therefore has a broad applicability domain.View Full Text

systems biology↗

Evidence for two main domestication trajectories in Saccharomyces cerevisiae linked to distinct bread-making processes

Despite bread being one of the most historically and culturally important fermented products, its history and influence on the evolution of associated microbial species remains largely unknown. The first evidence of leavened bread dates to the second millenium BCE in Egypt and since, the art of bread-making developed and spread worldwide. Nowadays, leavened bread is made either by using a pure commercial culture of the yeast Saccharomyces cerevisiae or by propagating a sourdough, which is a mix of flour and water spontaneously fermented by yeast and bacteria. We studied the domestication of S. cerevisiae populations originating from industry and sourdough and tested whether these different bread-making processes led to population divergence. We found that the origin of S. cerevisiae bakery strains is polyphyletic with 67 % of strains clustering in two main clades: most commercial strains were tetraploid and clustered with strains having diverse origins, including beer. By contrast, most sourdough strains were diploids and found in a second clade of strains having mosaic genomes and diverse origins including fruits, or clinical and wild environments. When compared to the others, sourdough strains harboured in average a higher copy number of genes involved in maltose utilization, a common sugar produced from dough starch. Overall, a high level of gene flow from multiple contributors was detected. Phenotyping of bakery and non bakery strains further showed that sourdough and industrial bakery populations have undergone human selection for rapidly starting fermentations and for high CO2 production. Interestingly, sourdough strains also showed a better adaptation to a sourdough mimicking environment, suggesting that natural selection occurred as well. In summary, our results revealed that the domestication of bakery yeast populations has been accompanied by dispersion, hybridization and divergent selection through industrial and artisanal bakery processes. In addition, they unveiled for the first time a case of fungus domestication where species divergence occurred through autotetraploidisation.

genomics↗

Artisanal and farmers bread making practices differently shape fungal species diversity in French sourdoughs

AO_SCPLOWBSTRACTC_SCPLOWPreserving microbial diversity in food systems is one of the many challenges to be met to achieve food security and quality. Although industrialization led to the selection and spread of specific fermenting microbial strains, there are still ongoing artisanal processes that may allow the conservation of a wider species diversity and genetic diversity. We examined whether the diversity of artisanal practices could lead to an increased level in fungal species diversity for bread making. We used an interdisciplinary participatory research approach including bakers, psycho-sociologists and microbiologists to analyze French bread making practices and describe fungal communities in naturally fermented sourdough of 27 bakers and 12 farmer bakers. Bread making practices were classified in two groups: the farmer-like practice group and the artisanal-like practice group. The well-known bakery yeast, Saccharomyces cerevisiae, was dominant (i.e. with a relative abundance over 50%) in only 24% of sourdoughs while other yeast species, belonging to the Kazachstania genus, were dominant in 54% of sourdoughs. Bread making practices were found to drive the distribution of fungal species across sourdoughs. The most striking bread making practice effect was the occurrence of Kazachstania humilis in sourdoughs made with artisanal-like practices and the occurrence of Kazachstania bulderi in sourdoughs made with farmer-like practices. Phenotypic divergences between sourdough and nonsourdough strains were found for K. humilis but not for K. bulderi. Overall, our results showed that preserving bread making practice diversity allows the preservation of a higher species and phenotypic diversity in microbial communities.

ecology↗

Kinetic analysis of yeast-yeast interactions in oenological conditions

Fermentation by microorganisms is a key step in the production of traditional food products such as bread, cheese, beer and wine. In these fermentative ecosystems, microorganisms interact in various ways, namely competition, predation, commensalism and mutualism. Traditional wine fermentation is a complex microbial process performed by Saccharomyces and non-Saccharomyces (NS) yeast species. To better understand the different interactions occurring within wine fermentation, isolated yeast cultures were compared with mixed co-cultures of one reference strain of S. cerevisiae with one strain of four NS yeast species (Metschnikowia pulcherrima, M. fructicola, Hanseniaspora opuntiae and H. uvarum). In each case, we studied population dynamics, resource consumed and metabolites produced from central carbon metabolism. This phenotyping of competition kinetics allowed us to confirm the main mechanisms of interaction between strains of four NS species. S. cerevisiae competed with H. uvarum and H. opuntiae for resources although both Hanseniaspora species were characterized by a strong mortality either in isolated or mixed fermentations. M. pulcherrima and M. fructicola displayed a negative interaction with the S. cerevisiae strain tested, with a decrease in viability in co-culture, probably due to iron depletion via the production of pulcherriminic acid. Overall, this work highlights the importance of measuring specific cell populations in mixed cultures and their metabolite kinetics to understand yeast-yeast interactions. These results are a first step towards ecological engineering and the rational design of optimal multi-species starter consortia using modeling tools. In particular the originality of this paper is for the first times to highlight the joint-effect of different species population dynamics on glycerol production and also to discuss on the putative role of lipid uptake on the limitation of some non-conventional species growth although interaction processes.

microbiology↗

The geometry of heterosis

Heterosis, the superiority of hybrids over their parents for quantitative traits, represents a crucial issue in plant and animal breeding. Heterosis has given rise to countless genetic, genomic and molecular studies, but has rarely been investigated from the point of view of systems biology. We hypothesized that heterosis is an emergent property of living systems resulting from frequent concave relationships between genotypic variables and phenotypes, or between different phenotypic levels. We chose the enzyme-flux relationship as a model of the concave genotype-phenotype (GP) relationship, and showed that heterosis can be easily created in the laboratory. First, we reconstituted in vitro the upper part of glycolysis. We simulated genetic variability of enzyme activity by varying enzyme concentrations in test tubes. Mixing the content of \"parental\" tubes resulted in \"hybrids\", whose fluxes were compared to the parental fluxes. Frequent heterotic fluxes were observed, under conditions that were determined analytically and confirmed by computer simulation. Second, to test this model in a more realistic situation, we modeled the glycolysis/fermentation network in yeast by considering one input flux, glucose, and two output fluxes, glycerol and acetaldehyde. We simulated genetic variability by randomly drawing parental enzyme concentrations under various conditions, and computed the parental and hybrid fluxes using a system of differential equations. Again we found that a majority of hybrids exhibited positive heterosis for metabolic fluxes. Cases of negative heterosis were due to local convexity between certain enzyme concentrations and fluxes. In both approaches, heterosis was maximized when the parents were phenotypically close and when the distributions of parental enzyme concentrations were contrasted and constrained. These conclusions are not restricted to metabolic systems: they only depend on the concavity of the GP relationship, which is commonly observed at various levels of the phenotypic hierarchy, and could account for the pervasiveness of heterosis.

systems biology↗