Prokaryotic photoperiodism: from molecules to evolution

细菌关心季节吗？鸟类迁徙，哺乳动物冬眠，植物开花，昆虫滞育：事实上，真核生命树的几乎所有分支都进化出了反应，使它们能够根据季节的变化而改变自己的行为和生理。这通常是通过一种称为光周期的现象发生的，在这种现象中，一天的长度是触发这些变化的环境因素。光周期是一种被广泛研究的现象，它是生物体生命及其与其他物种相互作用的重要事件的基础。它还直接受到气候变化的影响，因为温度和其他天气变量的变化可能会使以前有益的光周期反应不适应。确定光周期反应在气候变化下将如何变化是当务之急，但目前我们缺乏能够让我们直接测试这一点的模型生物，因为它们通常较长的生命周期到目前为止排除了实验进化光周期的尝试。在我攻读博士学位期间，我及时发现细菌也能够做出光周期反应。与哺乳动物的短日诱导冬眠类似，当细长聚球藻PCC7942--一种在昼夜节律领域内的显著蓝藻模式生物--的细胞暴露在短促的冬季白天时，它们在冰冻温度下的生存能力是暴露在漫长的夏季白天的细胞的2-3倍。在我的整个博士学位期间，我一直在描述这种反应的生理学特征，并了解到它的功能与真核细胞的光周期作用非常相似，尽管它们之间存在巨大的系统发育距离。值得注意的是，这种反应依赖于功能生物钟的存在，需要几代人才能形成，并涉及脂膜饱和度的预期变化。这项提议的首要目标是利用这一惊人的发现，建立蓝藻作为研究光周期进化的第一个细菌模型。蓝藻由于其快速的繁殖时间、简单的基因组和系统的生物钟特征，是一种独特的模式生物，它不仅可以确定光周期的机制特征，而且可以在不同的条件下进行实验进化。在这项提案中，我打算通过三个不同的战略来实现这一点。首先，我将使用大量可用于聚球藻的分子工具，通过RNAseq和转座子测序建立蓝藻光周期的遗传基础，以及使用蛋白质组学来确定除抗寒性之外的其他可能也是光周期的反应。其次，我将测试不同的蓝藻和其他模式细菌，以确定原核生物中光周期现象在系统发育中的分布情况，以及蓝藻是否也可以成为研究纬度跃迁的模式。最后，我将根据政府间气候变化专门委员会提出的最新模型，对蓝藻在气候变化条件下进行实验进化，并建立蓝藻和其他生物在试图适应气候变化强加给它们的新环境时可能采取的进化路径。总而言之，这些目标将快速推进光周期及其过去和未来演变的研究，为理解和减轻气候变化对光周期反应的影响提供新的工具。

Do bacteria care about the seasons? Birds migrate, mammals hibernate, plants flower, insects undergo diapause: in fact, almost all branches of the eukaryotic tree of life have evolved responses that allow them to alter their behavior and physiology in anticipation of the changing seasons. This usually happens through a phenomenon called photoperiodism, in which the length of the day is the environmental factor responsible for triggering these changes. Photoperiodism is a well-studied phenomenon that underlies important events in an organism's life and its interactions with other species. It is also directly affected by climate change, as changes in temperature and other weather variables can render a previously beneficial photoperiodic response maladaptive. Establishing how photoperiodic responses will change under climate change is an imperative, but currently we lack model organisms that allow us to directly test this, as their generally lengthy life cycles have so far precluded attempts at experimentally evolving photoperiodism. During my PhD, I made the timely discovery that bacteria are also capable of photoperiodic responses. Similar to short-day induced hibernation in mammals, when cells of Synechococcus elongatus PCC 7942 - a remarkable cyanobacterial model organism within the field of circadian rhythms - are exposed to short, winter-like days, they are capable of surviving freezing temperatures 2-3x better than counterparts that are exposed to long, summer-like days. Throughout my PhD, I have physiologically characterized this response and learned that it functions rather similarly to eukaryotic photoperiodism, despite their vast phylogenetic distance. Remarkably, this response is dependent upon the presence of a functional circadian clock, takes multiple generations to be formed, and involves anticipatory changes in lipid membrane saturation. The overarching goal of this proposal is to harness this striking discovery and establish cyanobacteria as the first bacterial model for studying the evolution of photoperiodism. Due to their fast generational time, simple genome and systematically characterized circadian clock, cyanobacteria are a unique model organism that would allow us to not only determine the mechanistic features of photoperiodism, but also would make it possible to perform experimental evolution under various conditions. In this proposal, I intend to make this possible by three separate strategies. First, I will use the vast array of molecular tools available for Synechococcus and establish the genetic basis of cyanobacterial photoperiodism through RNAseq and transposon sequencing, as well as use proteomics to determine other responses beyond cold resistance that may also be photoperiodic. Second, I will test different cyanobacteria and other model bacteria to establish how phylogenetically widespread photoperiodism is amongst prokaryotes, and whether cyanobacteria could also be a model for the study of latitudinal clines. Finally, I will perform experimental evolution on cyanobacteria under climate change conditions based on the latest models proposed by the Intergovernmental Panel on Climate Change and establish the evolutionary pathways that cyanobacteria and other organisms might take as they try to adapt to the new environments forced upon them by climate change. Taken together, these aims will fast-forward the study of photoperiodism and its past and future evolution, providing new tools to understand and mitigate the effects of climate change upon photoperiodic responses in general.