Diel expression dynamics in filamentous cyanobacteria

ABSTRACT Filamentous cyanobacteria of the Nostocaceae family can differentiate into multicellular forms to adapt to environmental stresses, and members can establish symbiosis with various embryophytes. Representative laboratory strains are typically grown under continuous light to maintain stable metabolic conditions; however, this departure from a natural diel cycle can result in extended stress. Early genomic examination of Nostoc punctiforme suggests the genetic potential for a circadian clock, but we lack insight into global cellular dynamics through the natural diel cycle for this model organism. Here, we comprehensively assess changes in expression of core cellular processes and the mobilome of accessory genetic elements during diel growth of N. punctiforme PCC 73102. The primary transcriptome confirmed that multicellular cyanobacteria precisely coordinate photosynthesis and carbon assimilation for cell division during the day, while control of DNA recombination and repair appeared to be sequestered to darkness. Moreover, we expanded the known repertoire of light-sensing proteins to uncover a putative regulator of circadian rhythm that itself exhibits striking oscillation between day-night expression. This was in sharp contrast to the arrhythmic pattern observed for a homolog of the canonical circadian input kinase in unicellular cyanobacteria. Looking beyond cellular coordination of diel growth, we uncovered dynamic mobile elements and, notably, targeted hypermutation by retroelements that are likely maintained for conflict mitigation, which is crucial for a multicellular lifestyle. IMPORTANCE Model strains of filamentous cyanobacteria are typically cultivated under controlled laboratory conditions that poorly reflect the natural environment, including growth under constant light. Our study addresses this discrepancy to provide a new benchmark for investigating gene expression in the model organism, Nostoc punctiforme . By analyzing changes in the global transcriptome over a diel cycle, we found a clear partition of cellular processes between periods of light and darkness, with metabolism dominating in the light and cell maintenance and repair processes dominating in the dark. In addition, an active mobilome of genetic elements was uncovered with dynamic expression patterns throughout a diel cycle. Our findings highlight the importance of considering diel cycles in cyanobacterial research and provide new insight into the regulatory complexity, genome plasticity, and adaptive mechanisms of these ecologically important organisms. Our study reinforces the need to consider the natural diel cycle in laboratory models of filamentous cyanobacteria, bringing new insights into their regulatory complexity and revealing adaptive drivers of genome plasticity that may enable members of Nostoc to occupy a wide variety of ecosystems.