Hagman Arne, Piškur Jure
Department of Biology, Lund University, Lund, Sweden.
PLoS One. 2015 Jan 24;10(1):e0116942. doi: 10.1371/journal.pone.0116942. eCollection 2015.
Baker's yeast Saccharomyces cerevisiae rapidly converts sugars to ethanol and carbon dioxide at both anaerobic and aerobic conditions. The later phenomenon is called Crabtree effect and has been described in two forms, long-term and short-term effect. We have previously studied under fully controlled aerobic conditions forty yeast species for their central carbon metabolism and the presence of long-term Crabtree effect. We have also studied ten steady-state yeast cultures, pulsed them with glucose, and followed the central carbon metabolism and the appearance of ethanol at dynamic conditions. In this paper we analyzed those wet laboratory data to elucidate possible mechanisms that determine the fate of glucose in different yeast species that cover approximately 250 million years of evolutionary history. We determine overflow metabolism to be the fundamental mechanism behind both long- and short-term Crabtree effect, which originated approximately 125-150 million years ago in the Saccharomyces lineage. The "invention" of overflow metabolism was the first step in the evolution of aerobic fermentation in yeast. It provides a general strategy to increase energy production rates, which we show is positively correlated to growth. The "invention" of overflow has also simultaneously enabled rapid glucose consumption in yeast, which is a trait that could have been selected for, to "starve" competitors in nature. We also show that glucose repression of respiration is confined mainly among S. cerevisiae and closely related species that diverged after the whole genome duplication event, less than 100 million years ago. Thus, glucose repression of respiration was apparently "invented" as a second step to further increase overflow and ethanol production, to inhibit growth of other microbes. The driving force behind the initial evolutionary steps was most likely competition with other microbes to faster consume and convert sugar into biomass, in niches that were semi-anaerobic.
面包酵母酿酒酵母在厌氧和好氧条件下都能迅速将糖类转化为乙醇和二氧化碳。后一种现象被称为克拉布特里效应，有长期和短期两种形式。我们之前在完全受控的好氧条件下研究了40种酵母的中心碳代谢以及长期克拉布特里效应的存在情况。我们还研究了10种稳态酵母培养物，用葡萄糖对它们进行脉冲处理，并跟踪动态条件下的中心碳代谢和乙醇的出现情况。在本文中，我们分析了那些湿实验室数据，以阐明决定不同酵母物种中葡萄糖命运的可能机制，这些酵母物种涵盖了大约2.5亿年的进化历史。我们确定溢流代谢是长期和短期克拉布特里效应背后的基本机制，它大约在1.25亿至1.5亿年前起源于酿酒酵母谱系。溢流代谢的“发明”是酵母有氧发酵进化的第一步。它提供了一种提高能量产生速率的通用策略，我们发现这与生长呈正相关。溢流的“发明”同时也使酵母能够快速消耗葡萄糖，这一特性可能是为了在自然界中“饿死”竞争对手而被选择的。我们还表明，呼吸作用的葡萄糖抑制主要局限于酿酒酵母以及在不到1亿年前全基因组复制事件后分化出来的密切相关物种中。因此，呼吸作用的葡萄糖抑制显然是作为第二步“发明”的，以进一步增加溢流和乙醇产量，抑制其他微生物的生长。最初进化步骤背后的驱动力很可能是与其他微生物竞争，以便在半厌氧生态位中更快地消耗和转化糖分成为生物量。
