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Review
.2022 Feb 11:12:815847.
doi: 10.3389/fphys.2021.815847. eCollection 2021.

Spectres of Clock Evolution: Past, Present, and Yet to Come

Affiliations
Review

Spectres of Clock Evolution: Past, Present, and Yet to Come

Maria Luísa Jabbur et al. Front Physiol..

Abstract

Circadian clocks are phylogenetically widespread biological oscillators that allow organisms to entrain to environmental cycles and use their steady-state phase relationship to anticipate predictable daily phenomena - such as the light-dark transitions of a day - and prepare accordingly. Present from cyanobacteria to mammals, circadian clocks are evolutionarily ancient and are thought to increase the fitness of the organisms that possess them by allowing for better resource usage and/or proper internal temporal order. Here, we review literature with respect to the ecology and evolution of circadian clocks, with a special focus on cyanobacteria as model organisms. We first discuss what can be inferred about future clock evolution in response to climate change, based on data from latitudinal clines and domestication. We then address our current understanding of the role that circadian clocks might be contributing to the adaptive fitness of cyanobacteria at the present time. Lastly, we discuss what is currently known about the oldest known circadian clock, and the early Earth conditions that could have led to its evolution.

Keywords: bacterial rhythms; biological timekeeping; circadian rhythms; evolution and climate change; evolution of circadian clocks; photoperiodism.

Copyright © 2022 Jabbur and Johnson.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Changes in temperature will likely affect temporal niches.(A) Average sea surface temperature (°C) across 34 years (1981–2015) for different latitudes, divided by seasons. Darker colours indicate more recent years.(B) Close-up of latitudes 45–70 from the first plot. For these latitudes, the effect of temperature increase seems to be the highest, particularly around summer and fall. In the summer, these temperature increases can be equivalent to a latitudinal shift of almost 5° toward the equator. The temperature data was provided by the NOAA/OAR/ESRL PSL, Boulder, CO, United States, OISST Version 2 (Reynolds et al., 2007), obtained through the International Research Institute/Lamont-Doherty Earth Observatory (IRI/LDEO) Climate Data Library.(C) Change in mean temperature and in the amplitude of the daily and yearly temperature cycle for different latitudinal bands. Data modified and redrawn from Wang and Dillon (2014).(D) Diagram showing the possible effects of an upwards shift in temperature in the temporal niche of a population. The central bell-shaped curve illustrates the annual change in photoperiod as a function of the month of the year. The black bar on they-axis and the grey shaded area represents the temperature range tolerated by the species. Blue and pink curves represent the yearly temperature cycle for a “baseline” scenario (blue) and a scenario in which the average temperatures increase slightly but the yearly temperature variation decreases (pink), such as in the temperate zone in(C). Blue and pink bars on the abscissa refer to the scenarios explained before and represent the time of the year in which that species is present (e.g., not in summer diapause), based on whether the temperature at the time is within its tolerated temperature range. Dashed lines indicate the photoperiod which anticipates a change from a thermally tolerable to a thermally intolerable condition.
FIGURE 2
FIGURE 2
Diagram showing the results of experiments done previously to test the adaptive value of the circadian clock in cyanobacteria(first andsecond row), as well as a proposed experiment(third row). Experiments in the first row refer to publications described in the text (Ouyang et al., 1998; Woelfle et al., 2004; Ma et al., 2013), and show that resonance between the circadian period (FRP = free-running period) and the environmental period increases cyanobacterial fitness, while no difference was observed in constant conditions (LL). Experiments in the second row are explained in more detail in the text (Woelfle et al., 2004; Ma et al., 2013), and show that cyanobacteria with circadian clocks outcompete clock-less cyanobacteria in rhythmic (LD) but not in constant (LL) conditions. This latter result was unexpected given the typical bias among chronobiologists that circadian clocks would be able to increase fitness by facilitating proper internal temporal order. The last row features an experiment that is yet to be reported, namely, interspecific competitions between different species of cyanobacteria. A possible prediction of this experiment is that the co-existence or not of the two species would be modulated by the environmental rhythmic conditions, and perhaps by the two species’ circadian clocks.
FIGURE 3
FIGURE 3
Evolution of the cyanobacterial circadian clock genes.(A) Timeline of the evolution of the three core cyanobacterial clock genes,kaiA,kaiB, andkaiC, compared with the timing of the Great Oxidation Event [in green, oxygen levels in relationship to today’s atmosphere (based on Lyons et al., 2014)], and the evolution of Eubacteria (timing based on estimates by TimeTree (Hedges et al., 2015; Marin et al., 2016) added for evolutionary context. The date of the origin ofkaiA is directly extracted from recent studies (Dvornyk and Mei, 2021), while dates forkaiB andkaiC are based on previous work (Dvornyk et al., 2003) after adjusting for the most current estimates of the origin of Cyanobacteria. All taxons represented in the figure contain copies ofkaiC, although not all groups withkaiC are shown, and non-kaiC-containing groups are not included for simplicity. Labels shown in red are bacterial groups that have a KaiBC-based timer [a KaiABC-based circadian clock in the case of Cyanobacteria, and a KaiBC “proto-clock” (hourglass timer?) in the case ofRhodopseudomonas (Ma et al., 2013)]. Blue-font labels indicate other Eubacteria in which a potential circadian clock has been described:Bacillus subtillis (Firmicutes) andKlebsiella aerogenes (Gammaproteobacteria). The origin of cyanobacteria is based on estimates by Blank and Sanchez-Baracaldo (2010), which is in general agreement with other reports. LUCA refers to the Last Unique Common Ancestor.(B) Protein tree of KaiC and other proteins in the RecA/DnaB superfamily (based on Leipe et al., 2000; Makarova and Koonin, 2017).
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