Diel cycle and circadian clocks in prokaryotes

Abstract

Diel cycle imposes daily oscillations in environmental conditions, which temporally structures most ecosystems. One of the most outstanding adaptations to this recurrent phenomenon is probably the emergence of time-keeping mechanisms – circadian clocks – that allow the organisms to synchronize their biological activities with daily variations. While circadian clocks are ubiquitous in Eukaryotes, they are so far only characterized in Cyanobacteria within Prokaryotes. However, growing evidence suggests that circadian clocks are widespread in the bacterial and archaeal domains. Studying the impact of diel cycle on Prokaryotes and deciphering their time-keeping mechanisms is of enormous biological importance as bacteria and archaea are crucial in all ecosystems and are essential to human health. Understanding their daily rhythms will undoubtedly provide numerous valuable insights in medical research, environmental sciences, and biotechnology. In this thesis, we assessed for the first time the impact of diel cycle on the functionality of marine picoplanktonic communities using a metaproteomic approach. Metaproteomics is a powerful tool that allows pertinent establishment of phenotype-genotype linkages, but despite its rapid development, this technology still faces many technical challenges that hamper its potential power. In this context, we developed mPies, a novel bioinformatic tool that addresses critical bioinformatic issues in the environmental metaproteomics, and we showed the importance of diversifying the experimental workflow for comprehensive metaproteomic studies. This methodological optimization helped us to compare the in-situ diel metaproteomic patterns of picoplanktonic communities sampled from the surface north-west Mediterranean Sea. Our data showed a taxa-specific response to diel cycle in the photoautotroph Synechococcales and in (photo)-heterotrophic bacteria such as Flavobacteriales, Pelagibacterales and Rhodobacterales. Next, we investigated the taxonomic distribution of circadian clock proteins in Prokaryotes, and we updated the list of bacteria and archaea of great ecological and industrial relevance that could potentially be clock-controlled. Based on this review, we choose to study the diel cycle impact and the circadian genes expression of the biotech promising Rhodospirillum rubrum. Our results showed that light and dark cycles induced broad regulation of its proteome and affected the regulation of kai genes at both transcriptional and translational levels. Overall, this work evidenced that diel cycle impacts the functionality of prokaryotes and reinforced the hypothesis of time-keeping mechanisms beyond Cyanobacteria.