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Kirchmayr, M. R.

Publications and source records attributed to Kirchmayr, M. R..

5 recordsLinked to original sources

Widespread Saccharomyces hybridization in agave fermentations arises repeatedly from asymmetric parental diversity

Interspecific hybridization can profoundly reshape genomes by bringing together divergent genetic backgrounds, yet its ecological and evolutionary dynamics remain poorly understood at the population level. Here, we identify an extensive hybridization system in traditional agave fermentations across Mexico involving Saccharomyces cerevisiae, a species frequently associated with human-managed environments, and its predominantly wild relative S. paradoxus. A genomic survey reveals unexpectedly high hybrid frequencies in geographically distant regions with contrasting environments. Targeted sampling of distilleries and surrounding natural sites reveals a strong ecological bias, with hybrids recovered almost exclusively from distilleries, although both parental species occur in anthropogenic and natural habitats. Hybrid genomes show extensive architectural diversity, including distinct ploidies, variable parental genome contributions, variable patterns of heterozygosity, and contrasting mitochondrial ancestries. Phylogenomic and population-structure analyses of hybrid subgenomes demonstrate multiple independent origins. These recurrent events show pronounced asymmetry in parental genetic diversity. Hybrids derive from several S. cerevisiae populations, already shaped by extensive introgression, whereas every S. paradoxus subgenome traces to a single genetically differentiated S. paradoxus lineage found exclusively in distilleries, an unexpected association for a predominantly wild species. These findings establish agave fermentations as an exceptional system for studying recurrent interspecific hybridization and reveal how pronounced asymmetry in parental ancestry can shape hybrid formation.

evolutionary biology↗

Domestication and deep lineage divergence define two discrete trajectories in Kluyveromyces marxianus

Although genomics has greatly improved our ability to detect population structure and genetic divergence, it remains difficult to determine when diversity within a recognized species reflects continuous variation and when it marks the emergence of discrete evolutionary lineages. In yeasts, population-genomic studies often reveal overlapping signatures of environmental association, admixture, and domestication, making this distinction especially challenging. By analyzing 178 globally sampled genomes from Kluyveromyces marxianus, an emerging yeast of biotechnological interest, we show that diversity within this species resolves into two contrasting evolutionary trajectories that do not map onto broad geographic origin. Most industrial and clinical isolates belong to a lineage marked by gene loss, aneuploidy, and reduced fertility, consistent with genomic hallmarks of domestication. In contrast, isolates confined to traditional agave fermentations in Mexico and South Africa form a highly distinct lineage, separated from the other lineages by up to 4.8% genome-wide nucleotide divergence, widespread reciprocal monophyly, no detectable recent gene flow, and reduced mating compatibility despite co-occurrence with other lineages. Together, these results show that within a single yeast species, domestication-associated genome remodeling and deep lineage divergence can define distinct trajectories, with implications for strain selection in biotechnology.

evolutionary biology↗

Hanseniaspora yeasts from agave fermentations provide insight into intraspecific gene loss

Hanseniaspora species stand out among yeasts for having the smallest genomes, marked by extensive gene family contractions. Consequently, they have been proposed as model organisms for studying the evolution of free-living cells lacking genes otherwise considered essential. Here, we show that Hanseniaspora yeasts are prevalent in agave fermentations used to produce traditional spirits across Mexico. We sequenced the genomes of 15 strains, unambiguously identifying them as H. lachancei, H. pseudoguilliermondii, H. guilliermondii, and H. opuntiae. Comparative genomic analyses revealed dynamic shifts in gene family sizes and compositions, suggesting ongoing gene loss within the fast-evolving branch of this genus. Notably, gene losses varied across functional categories, even among isolates of the same species. Growth assays across diverse stress conditions and carbon sources indicated that these genomic disparities do not directly translate into phenotypic differences. Together, our findings suggest that differential gene loss within species is an active evolutionary process shaping Hanseniaspora genomes, highlighting agave-fermentation populations as valuable models for studying genome reduction in a natural context.

genomics↗

Ecological divergence of sympatric Saccharomyces species across wild and fermentative environments in the neotropics

The common yeast Saccharomyces cerevisiae is widely associated with anthropogenic habitats and dominates agave fermentations in Mexico, despite the absence of starter cultures in artisanal production. Yet, the origins and dispersal of the microorganisms involved in this fermentation system--including wild S. cerevisiae and its sister species S. paradoxus--remain poorly understood. Here, we analyzed the distribution of these two species across three regions in Mexico by collecting a total of 861 samples from 15 traditional distilleries and 25 nearby natural sites, including tree bark, insects, fermentation tanks, and distillery surfaces. Among 4,006 isolates identified by MALDI-TOF biotyping, S. cerevisiae and S. paradoxus were recovered at overall rates of 21% and 3.4%, respectively, with the former more frequently found in distilleries and the latter in natural habitats. Notably, Saccharomyces isolates were not exclusively associated with oak trees, as strains were also recovered from leguminous, pine, and Anacardiaceae trees, suggesting that the oak specialization observed in temperate regions may not hold in tropical environments. Genome sequencing of 100 Saccharomyces isolates and SNP-based analyses showed that S. cerevisiae strains clustered by geography, not by substrate, and were largely confined to two Mexican Agave clades, with minor representation from the North American Oak, Pacific West Coast, and Wine clades. Strains isolated from agave fermentations belonged to the same populations as those from plant substrates, with insects, especially Drosophilidae, likely mediating their dispersal. Meanwhile, S. paradoxus isolates grouped into the SpA (Eurasian) and SpB (North American) lineages, with three novel SpB subclades identified. Intriguingly, one of these, the SpB_MxAgave population, was exclusively associated with agave fermentations, providing the first evidence of a persistent association of S. paradoxus with an anthropogenic habitat. Our study sheds light on the ecological dynamics and diversity of S. cerevisiae and S. paradoxus populations in the neotropics.

microbiology↗

Yeast diversity in open agave fermentations across Mexico

Yeasts are a diverse group of fungal microorganisms that are widely used to produce fermented foods and beverages. In Mexico, open fermentations are used to obtain spirits from agave plants. Despite the prevalence of this traditional practice throughout the country, yeasts have only been isolated and studied from a limited number of distilleries. To systematically describe the diversity of yeast species from open agave fermentations, here we generate the YMX.1.0 culture collection by isolating 4,524 strains from 68 sites in diverse climatic, geographical, and biological contexts. We used MALDI-TOF mass spectrometry for taxonomic classification and a subset of the strains was verified by ITS and D1/D2 sequencing. The most abundant species isolated from all producing regions were Saccharomyces cerevisiae, Pichia kudriavzevii, Pichia manshurica, and Kluyveromyces marxianus. Despite the great diversity of environmental conditions and production practices the composition of yeast communities remained largely homogeneous throughout locations and fermentation stages, even if less abundant but commonly occurring yeasts were considered. Furthermore, ITS and D1/D2 sequencing revealed two candidate new species of Saccharomycetales. To explore the intraspecific variation of the yeasts from agave fermentations, we conducted genome sequencing on four isolates of the non-conventional yeast Kazachstania humilis. The genomes of these four strains were considerably distinct from other genomes of the same species, suggesting that they belong to a different population. Our work contributes to the understanding and conservation of an open fermentation system of great cultural and economic importance, providing a valuable resource to study the biology and genetic diversity of microorganisms living at the interface of natural and human-associated environments. TAKE AWAYO_LIWe isolated and identified 4,524 yeast strains from open agave fermentations in Mexico. C_LIO_LIYeast communities remained largely homogeneous throughout diverse locations. C_LIO_LIKazachstania humilis genomes differed significantly from isolates in other regions of the world. C_LIO_LIWe report two candidate new species related to the Pichia clade. C_LI

microbiology↗