Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage.
Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage.
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DOI：
10.7554/elife.33034
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发表时间：
2018-04-12
期刊：
影响因子：
7.7
通讯作者：
Gonçalves P
中科院分区：
文献类型：
--
作者：
Gonçalves C;Wisecaver JH;Kominek J;Oom MS;Leandro MJ;Shen XX;Opulente DA;Zhou X;Peris D;Kurtzman CP;Hittinger CT;Rokas A;Gonçalves P
嗜果性是一种罕见的特征，包括对果糖的偏好超过其他碳源。在这里，我们表明，在由在高糖花生态位中繁衍生息的嗜果物种组成的酵母谱系（Wickerhamiella/Starmerella，W/S clade）中，嗜果性的获得与中心碳代谢的更广泛重塑同时进行。将比较基因组学与生化和遗传学方法相结合，我们收集了充足的证据，证明 W/S 进化枝的祖先中酒精发酵能力的丧失，以及随后通过水平获取同源细菌基因或修改预先存在的酵母基因而恢复的证据。蔗糖同化所需的酶也是从细菌中获得的，这表明在 W/S 进化枝中发现的遗传新颖性可能与对高糖环境的适应有关。这项工作展示了 HGT 事件的激增如何重塑中心碳代谢。细胞按照基因中包含的指令构建其组件，例如帮助它们从环境中获取能量的分子机器。这种遗传信息通常从父母传递给后代。在几代人的过程中，基因可以积累微小的变化，它们编码的分子可以获得新的角色：然而，这个过程通常很慢。然而，某些生物体也可以通过从其他物种“窃取”基因来获得全新的基因。例如，酵母，例如用于制作面包和啤酒的酵母，可以从附近的细菌中获取基因。这种“水平基因转移”有助于生物体快速获得新特征，如果环境快速变化，这尤其有用。酵母获得所需能量的一种方法是通过酒精发酵过程分解糖。为此，大多数酵母物种更喜欢使用一种称为葡萄糖的糖，但一小部分“嗜果糖”物种更喜欢使用一种称为果糖的糖。科学家们并不确切知道嗜果酵母是如何形成的，但有一些证据表明水平基因转移可能参与了这一过程。现在，贡萨尔维斯等人。将嗜果酵母的遗传物质与其他酵母群的遗传物质进行了比较。比较遗传物质有助于科学家识别物种之间的相似性和差异，并提供有关为什么特定遗传特征首先进化的线索。实验表明，在其历史早期，嗜果酵母失去了允许它们进行酒精发酵的基因，可能是因为它们可以通过不同的方式获取能量。然而，在后来的某个时间点，这些酵母必须适应在花蜜这种富含糖分的环境中生存。然后，他们更喜欢果糖作为能量来源，可能是因为这种糖可以更有效地补偿酒精发酵的缺失。后来，酵母从附近的细菌获得了一个基因，使它们能够再次进行酒精发酵：这提高了它们利用花蜜中存在的其他糖的能力。当获得能量时，酵母和其他生物体会产生与工业相关的物质。研究自然进化过程可以帮助科学家了解生物体如何改变其获取能量的方式并适应新的挑战。反过来，这有助于将酵母改造为“细胞工厂”，以环保且经济高效的方式生产有价值的化学品。
Fructophily is a rare trait that consists of the preference for fructose over other carbon sources. Here, we show that in a yeast lineage (the Wickerhamiella/Starmerella, W/S clade) comprised of fructophilic species thriving in the high-sugar floral niche, the acquisition of fructophily is concurrent with a wider remodeling of central carbon metabolism. Coupling comparative genomics with biochemical and genetic approaches, we gathered ample evidence for the loss of alcoholic fermentation in an ancestor of the W/S clade and subsequent reinstatement through either horizontal acquisition of homologous bacterial genes or modification of a pre-existing yeast gene. An enzyme required for sucrose assimilation was also acquired from bacteria, suggesting that the genetic novelties identified in the W/S clade may be related to adaptation to the high-sugar environment. This work shows how even central carbon metabolism can be remodeled by a surge of HGT events. Cells build their components, such as the molecular machinery that helps them obtain energy from their environment, by following the instructions contained in genes. This genetic information is usually transferred from parents to offspring. Over the course of several generations, genes can accumulate small changes and the molecules they code for can acquire new roles: yet, this process is normally slow. However, certain organisms can also obtain completely new genes by ‘stealing’ them from other species. For example, yeasts, such as the ones used to make bread and beer, can take genes from nearby bacteria. This ‘horizontal gene transfer’ helps organisms to rapidly gain new characteristics, which is particularly useful if the environment changes quickly. One way that yeasts get the energy they need is by breaking down sugars through a process called alcoholic fermentation. To do this, most yeast species prefer to use a sugar called glucose, but a small group of ‘fructophilic’ species instead favors a type of sugar known as fructose. Scientists do not know exactly how fructophilic yeasts came to be, but there is some evidence horizontal gene transfers may have been involved in the process. Now, Gonçalves et al. have compared the genetic material of fructophilic yeasts with that of other groups of yeasts . Comparing genetic material helps scientists identify similarities and differences between species, and gives clues about why specific genetic features first evolved. The experiments show that, early in their history, fructophilic yeasts lost the genes that allowed them to do alcoholic fermentation, probably since they could obtain energy in a different way. However, at a later point in time, these yeasts had to adapt to survive in flower nectar, an environment rich in sugar. They then favored fructose as their source of energy, possibly because this sugar can compensate more effectively for the absence of alcoholic fermentation. Later, the yeasts acquired a gene from nearby bacteria, which allowed them to do alcoholic fermentation again: this improved their ability to use the other sugars present in flower nectars. When obtaining energy, yeasts and other organisms produce substances that are relevant to industry. Studying natural processes of evolution can help scientists understand how organisms can change the way they get their energy and adapt to new challenges. In turn, this helps to engineer yeasts into ‘cell factories’ that produce valuable chemicals in environmentally friendly and cost-effective ways.