Photosynthetic circadian rhythmicity patterns of Symbiodium , the coral endosymbiotic algae

Abstract

Biological clocks are self-sustained endogenous timers that enable organisms (from cyanobacteria to humans) to anticipate daily environmental rhythms, and adjust their physiology and behaviour accordingly. Symbiotic corals play a central role in the creation of biologically rich ecosystems based on mutualistic symbioses between the invertebrate coral and dinoflagellate protists from the genus Symbiodinium. In this study, we experimentally establish that Symbiodinium photosynthesis, both as a free-living unicellular algae and as part of the symbiotic association with the coral Stylophora pistillata, is ‘wired’ to the circadian clock mechanism with a ‘free-run’ cycle close to 24 h. Associated photosynthetic pigments also showed rhythmicity under light/dark conditions and under constant light conditions, while the expression of the oxygen-evolving enhancer 1 gene (within photosystem II) coincided with photosynthetically evolved oxygen in Symbiodinium cultures. Thus, circadian regulation of the Symbiodinium photosynthesis is, however, complicated as being linked to the coral/host that have probably profound physiochemical influence on the intracellular environment. The temporal patterns of photosynthesis demonstrated here highlight the physiological complexity and interdependence of the algae circadian clock associated in this symbiosis and the plasticity of algae regulatory mechanisms downstream of the circadian clock.

Uncovering Spatio-Temporal and Treatment-Derived Differences in the Molecular Physiology of a Model Coral-Dinoflagellate Mutualism with Multivariate Statistical Approaches

“…However, the predominant experimental factor leading to sample partitioning in the SHSTTE was time, rather than temperature. As Symbiodinium gene expression, and physiology in general, is known to be highly dynamic [30,33], this finding was not unexpected. Importantly though, the fact that the Symbiodinium response variables more significantly contributed to temporal variation in the SHSTTE, while host coral parameters led to a relatively greater partitioning of samples by temperature in the SHVTS, emphasizes that notion put forth by Mayfield & Gates [29] and others that it is important to consider both compartments of the coral-Symbiodinium endosymbiosis when attempting to gauge the molecular physiological response of the composite holobiont to environmental change.…”

“…Specifically, coral metabolism is temporally variable due to the periodic nature of light-driven photosynthesis [30][31][32], and metabolic hysteresis driven by dinoflagellate photosynthesis as a function of the light cycle surely contributed to the temporal variation observed in the SHSTTE. Circadian rhythm may also have accounted, in part, for the separation of the 6-and 24-hr samples in the SHSTTE [33]. The former were collected at 13:45, and, while stable, artificial light was used in this experiment, it is possible that the temporal gene expression signatures were driven by an entrained response to high light levels that would normally be experienced at such times.…”

Respiratory oxygen consumption in the seagrass Zostera marina varies on a diel basis and is partly affected by light

“…The following PAR irradiances (µmol photons m −2  s −1 ) were used in sequence (the duration of each irradiance is indicated in parentheses): 20 (1 h), 40 (1 h), 70 (2 h), 120 (2 h), 150 (4 h), 70 (2 h), 40 (1 h), and 20 (2 h), the light being turned on at 06:30 and turned off at 21:30 (15 h:9 h, light:dark). These light cycles were used for the first well over 5 days (“light”), followed by well over 3 days of complete darkness (“continuous darkness”), to detect the presence of a potential endogenous circadian rhythm that could cause variations in respiration in the absence of external triggers (this setup is commonly used, e.g., Pallas et al 1974; Hagemeyer and Waisel 1990; Sorek et al 2013). Leaves for O 2 measurements and RNA extraction were collected at 06:30, 10:00, 13:30, 17:00, 20:30, 00:00, and 03:15 (Table ESM2).…”

Comparing the diel vertical migration of Karlodinium veneficum (dinophyceae) and Chattonella subsalsa (Raphidophyceae): PSII photochemistry, circadian control, and carbon assimilation

“…Photosynthesis and PSII activity are known to show circadian rhythms in a number of phytoplankton [10]) including many dinoflagellates [38,75,76,86] and can continue with high amplitude in excess of 3 days in constant conditions [10,76]. In particular, the maximum quantum yield of PSII follows a circadian rhythm (e.g.…”

“…In particular, the maximum quantum yield of PSII follows a circadian rhythm (e.g. [82,62,86], and was initially thought to stem from PSII rather than downstream from the plastoquinone (PQ) pool or PSI [82]). Additionally, Sorek et al [86] noted that along with rhythms in F v /F m , transcription of the oxygen-evolving enhancer gene showed circadian rhythmicity in the dinoflagellate Symbiodinium sp., implying that PSII rhythmicity may be linked to the donor side of PSII.…”