Prokaryotic photoperiodism: from molecules to evolution

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.