Evolutionary insights into an ancient fungal transition from land to sea

Though fungi have largely been studied in the context of terrestrial niches, aquatic species that originated from terrestrial ancestors can be found across the fungal kingdom. To date, the mechanisms of these transitions from land to sea have remained poorly understood, and it is unclear what traits are associated with the specialization of a fungal to marine environments. Here we develop Kluyveromyces budding yeasts, sampled from terrestrial, estuarine, and marine niches, as a model for the evolution of fungi into the ocean. Comparative analyses of genomes from the genus revealed a contraction in genome size and gene number in aquatic Kluyveromyces compared to their terrestrial relatives, including at genes annotated in alcoholic fermentation. In laboratory culture, we uncovered evidence for phenotypic losses in aquatic Kluyveromyces species, namely compromised desiccation and cold resistance relative to the terrestrial clade. Aquatic Kluyveromyces also exhibited better salt tolerance than terrestrial species, reflecting an evolutionary gain consonant with their provenance from seawater. Furthermore, in molecular-evolution analyses, we found robust signal for positive selection in the aquatic Kluyveromyces lineage, most notably at genes annotated in respiration. We interpret these results under a model in which the release of ethanol, which allows yeasts in terrestrial niches to kill off bacterial competitors at close range, has little use in the water; aquatic Kluyveromyces thus evolved to lose fermentation but gained other metabolic and stress-tolerance innovations essential for fitness in the marine niche. We propose that the syndrome of genomic features and phenotypes in aquatic Kluyveromyces reflects broadly relevant mechanisms of evolutionary transitions by fungi into ocean environments.