Prokaryotic photoperiodism: from molecules to evolution

细菌会在乎季节吗？鸟类迁徙、哺乳动物冬眠、植物开花、昆虫滞育：事实上，真核生物生命之树的几乎所有分支都进化出了相应的反应，使它们能够根据季节的变化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，其中一天的长度是触发这些变化的环境因素。光周期现象是一种被充分研究的现象，它是生物体生命中重要事件及其与其他物种相互作用的基础。它也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使以前有益的光周期反应适应不良。确定光周期反应在气候变化下如何变化是一个必要的条件，但目前我们缺乏模式生物，使我们能够直接测试这一点，因为它们通常漫长的生命周期到目前为止排除了实验进化光周期的尝试。在读博士期间，我及时发现细菌也有光周期反应的能力。类似于哺乳动物中的短日照诱导冬眠，当细长聚球藻PCC 7942的细胞-昼夜节律领域内的一种显着的蓝藻模式生物-暴露于短的，冬季般的日子时，它们能够比暴露于长的，夏季般的日子的对应物更好地在冷冻温度下存活2- 3倍。在我的博士学位期间，我对这种反应进行了生理学上的描述，并了解到它的功能与真核生物的光周期性相当相似，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性生物钟的存在，需要多代才能形成，并涉及脂质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，并建立蓝藻作为研究光周期性进化的第一个细菌模型。由于其快速的世代时间，简单的基因组和系统特征的昼夜节律钟，蓝藻是一个独特的模式生物，这将使我们不仅能够确定光周期的机制特征，而且还可以在各种条件下进行实验进化。在本建议中，我打算通过三个不同的战略来实现这一目标。首先，我将使用聚球藻可用的大量分子工具，并通过RNAseq和转座子测序建立蓝藻光周期性的遗传基础，以及使用蛋白质组学来确定除了抗寒性之外的其他反应，这些反应也可能是光周期性的。第二，我将测试不同的蓝藻和其他模式细菌，以建立如何在原核生物中广泛分布的光周期性，以及蓝藻是否也可以作为纬向倾斜的研究模型。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，在气候变化条件下对蓝藻进行实验性进化，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途径。总之，这些目标将加快光周期性及其过去和未来演变的研究，提供新的工具来理解和减轻气候变化对光周期反应的影响。

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.