Minimal tool set for a prokaryotic circadian clock

BMC Evol Biol. 2017 Jul 21;17(1):169. doi: 10.1186/s12862-017-0999-7.

Abstract

Background: Circadian clocks are found in organisms of almost all domains including photosynthetic Cyanobacteria, whereby large diversity exists within the protein components involved. In the model cyanobacterium Synechococcus elongatus PCC 7942 circadian rhythms are driven by a unique KaiABC protein clock, which is embedded in a network of input and output factors. Homologous proteins to the KaiABC clock have been observed in Bacteria and Archaea, where evidence for circadian behavior in these domains is accumulating. However, interaction and function of non-cyanobacterial Kai-proteins as well as homologous input and output components remain mainly unclear.

Results: Using a universal BLAST analyses, we identified putative KaiC-based timing systems in organisms outside as well as variations within Cyanobacteria. A systematic analyses of publicly available microarray data elucidated interesting variations in circadian gene expression between different cyanobacterial strains, which might be correlated to the diversity of genome encoded clock components. Based on statistical analyses of co-occurrences of the clock components homologous to Synechococcus elongatus PCC 7942, we propose putative networks of reduced and fully functional clock systems. Further, we studied KaiC sequence conservation to determine functionally important regions of diverged KaiC homologs. Biochemical characterization of exemplary cyanobacterial KaiC proteins as well as homologs from two thermophilic Archaea demonstrated that kinase activity is always present. However, a KaiA-mediated phosphorylation is only detectable in KaiC1 orthologs.

Conclusion: Our analysis of 11,264 genomes clearly demonstrates that components of the Synechococcus elongatus PCC 7942 circadian clock are present in Bacteria and Archaea. However, all components are less abundant in other organisms than Cyanobacteria and KaiA, Pex, LdpA, and CdpA are only present in the latter. Thus, only reduced KaiBC-based or even simpler, solely KaiC-based timing systems might exist outside of the cyanobacterial phylum, which might be capable of driving diurnal oscillations.

Keywords: Archaea; BLAST; Circadian clock; Co-occurrence; Cyanobacteria; Input factors; Kinase activity; Length distribution; Output factors.

MeSH terms

  • Amino Acid Motifs
  • Archaea / genetics
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Circadian Clocks / genetics*
  • Circadian Rhythm / genetics
  • Circadian Rhythm Signaling Peptides and Proteins / chemistry
  • Circadian Rhythm Signaling Peptides and Proteins / genetics
  • Conserved Sequence
  • Gene Expression Regulation, Bacterial
  • Genes, Bacterial
  • Phosphorylation
  • Phylogeny
  • Sequence Homology, Nucleic Acid
  • Synechococcus / genetics*
  • Synechococcus / physiology*
  • Transcriptome / genetics

Substances

  • Bacterial Proteins
  • Circadian Rhythm Signaling Peptides and Proteins
  • KaiB protein, cyanobacteria
  • KaiC protein, cyanobacteria

Associated data

  • figshare/10.6084/m9.figshare.3823902.v3
  • figshare/10.6084/m9.figshare.3823899.v3