From resonance to chaos: modulating spatiotemporal patterns through a synthetic optogenetic oscillator

Abstract

Oscillations are a recurrent phenomenon in biological systems across scales, including circadian clocks, metabolic oscillations and embryonic genetic oscillators. Despite their fundamental significance in biology, deciphering core principles of biological oscillators is very challenging due to the multiscale complexity of genetic networks and the difficulty in perturbing organisms in vivo. In this study, we tackle this challenge by re-designing the well-characterised synthetic oscillator, known as "repressilator", in Escherichia coli and controlling it using optogenetics, thus introducing the "optoscillator". When we apply periodic light pulses, the optoscillator behaves as a forced oscillator. Bacterial colonies harboring synthetic oscillators manifest oscillations as spatial ring patterns. Leveraging this feature, we systematically investigate the number, intensity and sharpness of the rings under different regimes of light exposure. By integrating experimental approaches with mathematical modeling, we show that this simple oscillatory circuit can generate complex dynamics that, depending on the external periodic forcing, are transformed into distinct spatial patterns. We report the observation of synchronisation, resonance, undertone and period doubling. Furthermore, we present evidence supporting the existence of a chaotic regime. This work highlights the intricate spatiotemporal patterns accessible by synthetic oscillators and underscores the potential of our approach in understanding the underlying principles governing biological oscillations.