Genomic signatures of adaptation to wine biological ageing conditions in biofilm‐forming flor yeasts

Abstract

The molecular and evolutionary processes underlying fungal domestication remain largely unknown despite the importance of fungi to bioindustry and for comparative adaptation genomics in eukaryotes. Wine fermentation and biological ageing are performed by strains of S. cerevisiae with, respectively, pelagic fermentative growth on glucose and biofilm aerobic growth utilizing ethanol. Here, we use environmental samples of wine and flor yeasts to investigate the genomic basis of yeast adaptation to contrasted anthropogenic environments. Phylogenetic inference and population structure analysis based on single nucleotide polymorphisms revealed a group of flor yeasts separated from wine yeasts. A combination of methods revealed several highly differentiated regions between wine and flor yeasts, and analyses using codon-substitution models for detecting molecular adaptation identified sites under positive selection in the high-affinity transporter gene ZRT1. The cross-population composite likelihood ratio revealed selective sweeps at three regions, including in the hexose transporter gene HXT7, the yapsin gene YPS6 and the membrane protein coding gene MTS27. Our analyses also revealed that the biological ageing environment has led to the accumulation of numerous mutations in proteins from several networks, including Flo11 regulation and divalent metal transport. Together, our findings suggest that the tuning of FLO11 expression and zinc transport networks are a distinctive feature of the genetic changes underlying the domestication of flor yeasts. Our study highlights the multiplicity of genomic changes underlying yeast adaptation to man-made habitats and reveals that flor/wine yeast lineage can serve as a useful model for studying the genomics of adaptive divergence.

Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution

“…By looking at rates of nonsynonymous substitutions, levels of differentiation and footprints of selective sweeps, Coi et al . () identified functions involved in the specific phenotypes of flor yeasts, forming a biofilm on wine during maturation. The functions involved in this specific adaptation included divalent metal transport and the level of expression of FLO11, a gene known to be involved in flocculation in wine yeast.…”

Many interspecific chromosomal introgressions are highly prevalent in Holarctic Saccharomyces uvarum strains found in human‐related fermentations

“…Observed heterozygosity ranged from 0 to 10%, the mostly heterozygous locus being 7_65. Interestingly, Almeida et al () discussed the possible selective advantage of chromosome 7 introgression, as it contains the FZF1 gene involved in sulphite resistance (Avram et al, ; Avram et al, ; Park et al, ) and the ZRT1 gene that presents traces of balancing selection (Coi et al, ). In this work, we show that chromosome 7 introgression is not significantly over‐represented in cider‐ and wine‐making processes compared with natural ones, in apparent contradiction to any selective advantage.…”

QTL mapping of modelled metabolic fluxes reveals gene variants impacting yeast central carbon metabolism

“…The parent strains of this segregant population are strain MTF2621 (haploid spore of 4CAR1 [ΔHO::Neo r ]) and MTF2622 (haploid spore of T73 [ΔHO::Nat r ]). Strain T73 belongs to the phylogenetic clade of wine strains, whereas strain 4CAR1 belongs to the group of champagne strains, which originated through crossings between strains of the wine clade and the flor clade 75 .…”