Evolution of ecological dominance of yeast species in high-sugar environments

In budding yeasts, fermentation in the presence of oxygen evolved around the time of a whole genome duplication (WGD) and is thought to confer dominance in high-sugar environments because ethanol is toxic to many species. While there are many fermentative yeast species, only Saccharomyces cerevisiae consistently dominates wine fermentations. In this study, we use co-culture experiments and intrinsic growth rate assays to examine the relative fitness of non-WGD and WGD yeast species across environments to assess when S. cerevisiae's ability to dominate high-sugar environments arose. We show that S. cerevisiae dominates nearly all other non-WGD and WGD species except for its sibling species S. paradoxus in both grape juice and a high-sugar rich medium. Of the species we tested, S. cerevisiae and S. paradoxus have evolved the highest ethanol tolerance and intrinsic growth rate in grape juice. However, the ability of S. cerevisiae and S. paradoxus to dominate certain species depends on the temperature and the type of high-sugar environment. Our results indicate that dominance of high-sugar environments evolved much more recently than the WGD, most likely just prior to or during the differentiation of Saccharomyces species, and that evolution of multiple traits contributes to S. cerevisiae's ability to dominate wine fermentations.

在出芽酵母（budding yeasts）中，有氧发酵的演化时间与全基因组复制（whole genome duplication, WGD）事件大致重合，该性状被认为可使酵母在高糖环境中占据竞争优势，因乙醇对多数物种具有毒性。尽管存在诸多发酵性酵母物种，但唯有酿酒酵母（Saccharomyces cerevisiae）始终在葡萄酒发酵过程中占据主导地位。本研究通过共培养实验（co-culture experiments）与本征生长速率测定实验（intrinsic growth rate assays），分析非全基因组复制（non-WGD）与全基因组复制（WGD）酵母物种在不同环境下的相对适合度，以此探究酿酒酵母（S. cerevisiae）获得高糖环境主导能力的演化节点。研究结果显示，在葡萄汁与高糖富集培养基两种环境中，酿酒酵母几乎可主导所有其他非WGD与WGD酵母物种，仅其姊妹物种帕拉酵母（Saccharomyces paradoxus）除外。在所测试的物种中，酿酒酵母与帕拉酵母在葡萄汁中演化出了最高的乙醇耐受性与本征生长速率。不过，二者对部分物种的主导能力，取决于环境温度与高糖环境的类型。本研究结果表明，酿酒酵母对高糖环境的主导能力的演化时间远晚于全基因组复制事件，极有可能恰好在酵母属（Saccharomyces）物种分化之前或分化过程中；而多性状的协同演化，共同促成了酿酒酵母在葡萄酒发酵中的主导地位。