Circadian phase alignment promotes survival under predictive oxidative stress
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Circadian clocks are endogenous time-keeping mechanisms that continue to oscillate with a period that approximates 24 h in the absence of cyclic environmental cues. This free-running period (FRP) varies from species to species and can vary within species across latitudinal clines. Because natural environments provide daily cues that reset circadian clocks to exactly 24 h, the importance of the FRP length is unclear. Using the cyanobacterium Synechococcus elongatus we show that the FRP length alters the alignment of a biological process with an environmental reference, known as phase angle of entrainment, across seasonal photoperiods, thereby repositioning stress-response programs relative to the external environment. This phase relationship affects the overall fitness of the organism: strains that position stress-response programs to peak at the time at which the stressor peaks outcompete their early- or late-peaking counterparts. Our results suggest that the FRP length is selected for its ability to adjust the phase angle of entrainment across seasonal photoperiods: the wild-type FRP length was uniquely plastic in its ability to adjust stress-response programs to coincide with the stressor in all photoperiod conditions.
Significance Statement
Circadian clocks are nearly universal biological timing systems that allow organisms to anticipate daily environmental changes, optimize environmental resources, and avoid environmental threats. We investigated which features of clock function promote survival fitness and which environmental conditions provide selection. A long-standing hypothesis is that the phase relationship between the internal timing mechanism and the external environment is critical for the circadian clock to confer a fitness advantage. However, because this phase relationship is influenced by the circadian period, tests of this hypothesis confound the two features. We experimentally decoupled the free-running period and the environmental phase relationship to show that the phase relationship, rather than the free-running period, confers fitness under environmental conditions that impose a selection.
