Bacteria can anticipate and adaptively respond to the seasons

Photoperiodic Time Measurement (PPTM) is the ability of plants and animals to measure differences in day/night-length (photoperiod, PP) and use that information to anticipate seasonal changes in key environmental factors such as annual changes in average temperature. This timekeeping phenomenon, which is well documented for higher organisms, enables processes such as gonadal growth/regression, flowering, hibernation, and diapause to optimally adapt to annual transformations of the environment. We discovered PPTM capability in cyanobacteria, which is unexpected since cyanobacteria are unicellular prokaryotes with generation times as short as 5-6 hours. Therefore PPTM is not confined to eukaryotes with long generation times. Here we show that cyanobacteria can distinguish between short and long daylengths (photoperiods) and respond to short winter-like days by developing an enhanced resistance to cold. This capability develops over several cycles of photoperiod, and therefore they harbor a “photoperiodic counter” that is a common characteristic of PPTM in higher organisms. These photoperiodic responses are dependent on the presence of the kaiABC genes that encode the central circadian clockwork in cyanobacteria. Short days that herald winter stimulated desaturation of membrane lipids, which is a seasonally adaptive response to lower temperatures. Long vs. short days evoke differential programs of gene transcription, including differential expression of stress response genes, suggesting that PPTM originally evolved from stresses that recur seasonally. Therefore, PPTM is a property of much simpler organisms than previously appreciated, with important implications for the evolution of biological timekeeping mechanisms. In our recent work, we describe that cyanobacteria are capable of anticipating seasonal changes and exhibit photoperiodic responses. To investigate what genes and pathways could be involved in the establishment of this response, we performed RNAseq in 1) wild-type and 2) circadian clock knock-outs (∆kaiABC) strains of the cyanobacterial model Synechococcus elongatus PCC 7942. We used two different photoperiods, 1) short-day (LD8:16, 8h of dark, 16h of darkness), which we demonstrate to be inducible of a photoperiodic resistance to cold, and 2) long-day (LD16:8), which does not induce increased cold resistance. As we observed that the photoperiodic response takes multiple cycles of LD to develop, we performed the RNAseq in samples collected after 1) 1 LD cycle, which is not sufficient to induce the response, 2) 4 LD cycles, which is sufficient to induce a complete response, and 3) 8 LD cycles, which is the condition most used throughout our manuscript. All samples were collected at their respective middays, and had been exposed to ~60h of light of 40µE m-2 s-1 intensity prior to collection.