Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments

Abstract

Circadian clocks display remarkable reliability despite significant stochasticity in biomolecular reactions. We study the dynamics of a circadian clock-controlled gene at the individual cell level in Anabaena sp. PCC 7120, a multicellular filamentous cyanobacterium. We found significant synchronization and spatial coherence along filaments, clock coupling due to cell-cell communication, and gating of the cell cycle. Furthermore, we observed low-amplitude circadian oscillatory transcription of kai genes comprising the post-transcriptional core oscillatory circuit, and high-amplitude oscillations of rpaA coding for the master regulator transducing the core clock output. Transcriptional oscillations of rpaA suggest an additional level of regulation. A stochastic, one-dimensional toy model of coupled clock cores and their phosphorylation states shows that demographic noise can seed stochastic oscillations outside the region where deterministic limit cycles with circadian periods occur. The model reproduces the observed spatio-temporal coherence along filaments, and provides a robust description of coupled circadian clocks in a multicellular organism.

Cut the noise or couple up: Coordinating circadian and synthetic clocks

“…This was strongly supported by genetic perturbation of the septal junctions connecting adjacent Anabaena sp. PCC 7210 cells, which resulted in much faster decay in spatial autocorrelation and significantly reduced order parameter (Arbel-Goren et al, 2021). Thus, these latest results have demonstrated that circadian coupling in cyanobacteria can exist, at least via direct cytoplasmic connections in filamentous species.…”

“…popular, particularly for single-cell-level observation (Chabot et al, 2007;Martins et al, 2016;Chew et al, 2018;Arbel-Goren et al, 2021).…”

“…Current understanding of clock coupling in cyanobacteria comes from three main studies (Mihalcescu et al, 2004;Amdaoud et al, 2007;Arbel-Goren et al, 2021). Mihalcescu, Hsing, and Leibler first reported in 2004 that no coupling exists between S. elongatus PCC 7942 clocks, concluded through tracking oscillations in PkaiBC-driven bioluminescence of agarose pad-grown single cells (Mihalcescu et al, 2004).…”

“…Excitingly, in contrast to the unicellular cyanobacteria so far discussed, a study has most recently found evidence for coupling in the filamentous multicellular cyanobacterium Anabaena sp. PCC 7120 (Arbel-Goren et al, 2021). Arbel-Goren et al found that individual cells expressing a fluorescent pecB CCG reporter within Anabaena sp.…”

Single-Cell Measurements of Fixation and Intercellular Exchange of C and N in the Filaments of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120

“…Because the cellular C/N balance is highly regulated in Anabaena ( 32 ), it is plausible that filaments of the WT that fixed little N were affected in CO 2 fixation, as observed for unicellular cyanobacteria after several hours of N deprivation ( 33 ). On the other hand, different filaments could exhibit dissimilar metabolic states because they can be at different positions in the circadian cycle, which runs in individual Anabaena filaments even under constant light ( 34 ). Thus, the possibility that stretches of vegetative cells with low photosynthetic activity provide a heterocyst with insufficient reduced C affecting N 2 fixation should also be considered.…”