Evolution of KaiC-Dependent Timekeepers: A Proto-circadian Timing Mechanism Confers Adaptive Fitness in the Purple Bacterium Rhodopseudomonas palustris

Ma, Peijun; Mori, Tetsuya; Zhao, Chuanxi; Thiel, Teresa; Johnson, Carl Hirschie

doi:10.1371/journal.pgen.1005922

Cited by 61 publications

(112 citation statements)

References 65 publications

(112 reference statements)

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“…Both proteins display autophosphorylation and KaiC2 from Rhodopseudomonas palustris shows elevated ATPase activity [59]. Nevertheless, the function of cyanobacterial KaiC2 and KaiC3 homologs remains unclear.…”

Section: Resultsmentioning

confidence: 99%

Minimal tool set for a prokaryotic circadian clock

Schmelling

Lehmann

Chaudhury³

et al. 2017

BMC Evol Biol

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BackgroundCircadian 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.ResultsUsing 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.ConclusionOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0999-7) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Minimal tool set for a prokaryotic circadian clock

Schmelling

Lehmann

Chaudhury³

et al. 2017

BMC Evol Biol

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“…This hypothesis is analogous to the fact that a pendulum with friction cannot be distinguished from a selfsustained oscillator when subjected to periodic external forces. Moreover, certain organisms such as yeast or purple bacteria use such degenerated circadian oscillators and are therefore unable to exhibit self-sustained rhythmicity under constant conditions, although rhythms are detected when exposed to an environment with daily variation (33,34). We further suspect that the emergence of mammalian circadian rhythms during differentiation of embryonic stem cells is mediated via Hopf bifurcation because the oscillation amplitude gradually increases during development (35).…”

Section: Discussionmentioning

confidence: 96%

Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation

Murayama

Kori

Oshima

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Cold temperatures lead to nullification of circadian rhythms in many organisms. Two typical scenarios explain the disappearance of rhythmicity: the first is oscillation death, which is the transition from self-sustained oscillation to damped oscillation that occurs at a critical temperature. The second scenario is oscillation arrest, in which oscillation terminates at a certain phase. In the field of nonlinear dynamics, these mechanisms are called the Hopf bifurcation and the saddle-node on an invariant circle bifurcation, respectively. Although these mechanisms lead to distinct dynamical properties near the critical temperature, it is unclear to which scenario the circadian clock belongs. Here we reduced the temperature to dampen the reconstituted circadian rhythm of phosphorylation of the recombinant cyanobacterial clock protein KaiC. The data led us to conclude that Hopf bifurcation occurred at ∼19°C. Below this critical temperature, the self-sustained rhythms of KaiC phosphorylation transformed to damped oscillations, which are predicted by the Hopf bifurcation theory. Moreover, we detected resonant oscillations below the critical temperature when temperature was periodically varied, which was reproduced by numerical simulations. Our findings suggest that the transition to a damped oscillation through Hopf bifurcation contributes to maintaining the circadian rhythm of cyanobacteria through resonance at cold temperatures.

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“…This is one simple example of why bacteria may have evolved timekeeping systems to coordinate metabolic events during the day to optimize performance and/or to temporally separate potentially conflicting metabolic processes. Whereas the timekeeper of cyanobacteria is well established as a prototypical circadian clock, other bacteria may have evolved alternative timekeeping systems, such as an , which confers a fitness advantage 14 .…”

mentioning

confidence: 99%

“…Therefore, bacteria that have a daily timekeeping mechanism, even if it is not a complete circadian system such as those found in cyanobacteria, probably have adaptive advantages. In this Review, we highlight recent mechanistic insights into circadian oscillators in cyanobacteria and timekeepers in other bacteria 14,18,19 . Moreover, we consider the potential adaptive value of both oscillating clocks and hourglass timers.…”

mentioning

confidence: 99%

Timing the day: what makes bacterial clocks tick?

et al. 2017

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Chronobiological studies of prokaryotic organisms have generally lagged far behind the study of endogenous circadian clocks in eukaryotes, in which such systems are essentially ubiquitous. However, despite only being studied during the past 25 years, cyanobacteria have become important model organisms for the study of circadian rhythms and, presently, their timekeeping mechanism is the best understood of any system in terms of biochemistry structural biology, biophysics and adaptive importance. Nevertheless, intrinsic daily rhythmicity among bacteria other than cyanobacteria is essentially unknown; some tantalizing information suggests widespread daily timekeeping among Eubacteria and Archaea through mechanisms that share common elements with the cyanobacterial clock but are distinct. Moreover, the recent surge of information about microbiome–host interactions has largely neglected the temporal dimension and yet daily cycles control important aspects of their relationship.

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Evolution of KaiC-Dependent Timekeepers: A Proto-circadian Timing Mechanism Confers Adaptive Fitness in the Purple Bacterium Rhodopseudomonas palustris

Cited by 61 publications

References 65 publications

Minimal tool set for a prokaryotic circadian clock

Minimal tool set for a prokaryotic circadian clock

Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation

Timing the day: what makes bacterial clocks tick?

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