Diel expression dynamics in filamentous cyanobacteria

Filamentous cyanobacteria of the Nostocaceae family are able to 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 regulator 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 to ensure conflict mitigation, which is crucial to a multicellular lifestyle. Overall design: To investigate global diel expression dynamics, we grew Nostoc punctiforme PCC 73102 / ATCC 29133 on a 12-hour light and 12-hour dark growth cycle for 9 days. Time points were chosen at transition stages (Pre-Dawn, Pre-Dusk), steady-state stages (MidLight, MidDark) for the first 8 days. At day 9, the cycle was disrupted and samples were maintained at either 24-hours of light (Light24) or 24-hours of dark (Dark24). Samples were collected in biological triplicate for all 12 time points.