Contrasting evolutionary trajectories of nitrate assimilation across Brettanomyces bruxellensis lineages

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Abstract Brettanomyces bruxellensis is a yeast species associated with diverse fermentation environments and characterized by extensive genetic diversity, including diploid, autotriploid, and allotriploid lineages resulting from independent hybridization events. These lineages are associated with distinct ecological niches and provide a framework for studying metabolic trait evolution in complex genomes. Nitrate assimilation is a relatively uncommon trait among yeasts and has been reported in B. bruxellensis , but its distribution and evolutionary history within the species remain poorly understood. Here, we combined phenotypic characterization of 151 strains with genomic analyses of 946 whole-genome sequences to investigate nitrate assimilation. Growth assays revealed that nitrate assimilation is widespread but unevenly distributed across genetic lineages, with some populations largely retaining the trait whereas others have frequently lost it. Genomic analyses identified extensive variation affecting the nitrate assimilation gene cluster composed of YNR1 , YNI1 , and YNT1 . Nitrate assimilation was strongly associated with both gene copy number and predicted gene functionality, with nitrate-assimilating strains generally carrying more functional copies of the cluster. Leveraging the complex genomic architecture of the species, we independently analyzed primary and acquired genomes in allotriploid lineages and uncovered contrasting evolutionary trajectories following hybridization. While nitrate assimilation genes were generally maintained in primary genomes, acquired genomes showed a higher prevalence of gene loss and predicted loss-of-function variants, revealing asymmetric dynamics between subgenomes. Altogether, our results suggest that nitrate assimilation represents an ancestral trait that has been differentially maintained across B. bruxellensis lineages through a combination of copy number variation, gene degeneration, and genome-specific evolutionary dynamics. These findings provide new insights into how genome architecture and polyploid evolution shape the maintenance and loss of metabolic traits in an industrially relevant yeast species. Author Summary Microorganisms adapt to new environments by gaining, modifying, or losing biological functions over evolutionary time. Understanding how these processes occur remains a central question in evolutionary biology, particularly in species with complex genomes. The yeast Brettanomyces bruxellensis provides an interesting model because it is associated with diverse fermentation environments and genetically distinct lineages with different evolutionary histories. We focused on nitrate assimilation, a relatively uncommon ability among yeasts that enables the use of nitrate as a nitrogen source. By combining growth experiments with large-scale genome analyses, we investigated how this trait is distributed across the species and how it evolved. We found that nitrate assimilation is likely an ancestral trait, but that it has been maintained or lost depending on the lineage. These differences are associated with variation in the number and integrity of genes involved in nitrate assimilation. B. bruxellensis also contains hybrid lineages carrying both primary and acquired genomes. By analyzing these genomes separately, we found that nitrate assimilation genes follow different evolutionary trajectories, with acquired genomes showing a greater tendency toward gene loss. Our results illustrate how hybridization and genome architecture can influence the maintenance or loss of biological functions within a species.

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