Extracellular pH Is Under Circadian Control inGonyaulax polyedraand Forms a Metabolic Feedback Loop

Abstract

This study investigates the relationship between the circadian clock and metabolism based on recordings of the extracellular pH in cultures of the marine dinoflagellate, Gonyaulax polyedra. In light-dark cycles, pH of the medium rises during the light phase and declines in the dark. The amplitude of this pH-rhythm correlates with light intensity, indicating photosynthesis (and respiration) as the driving force. The recorded extracellular pH changes probably reflect the need to control intracellular pH in spite of pH-modifying reactions. The daily pH-changes are under control of the circadian clock because they continue to oscillate with a circa-24 h period in constant light, albeit with a smaller amplitude. Similar to other circadian output rhythms, the pH rhythm depends (amplitude and phase) on nitrate levels in the medium. Both the bioluminescence and the pH rhythm can also be shifted by extracellular pH-changes although Gonyaulax is rarely exposed to significant pH changes in its marine ecosystems (except for highly dense algal blooms). Because intracellular proton levels are both affecting circadian input and output they form a feedback loop with the Gonyaulax circadian system indicating complex interactions between metabolism and the circadian clock.

Photosynthetic oscillation in individual cells of the marine diatom Coscinodiscus wailesii (Bacillariophyceae) revealed by microsensor measurements

“…Finally, comparison can be made with very much longerterm (diel) changes in extracellular pH noted in the dinoflagellate Gonyaulax polyedra (Eisensamer and Roennenberg 2004). As well as having a period some 600-700 times greater than the oscillations reported here, the dinoflagellate oscillations were not endogenous in single cells, but were observed in continuous illumination after entrainment of a cell population in diel light-dark cycles.…”

An External δ-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition

“…Total DIC ranged between 1.8 and 2.1 mmol/L as measured with a CO 2 ISE electrode (Analytical Sensors), and total alkalinity was approximately 2.1 mEq/L as measured by acid titration, conditions that resemble those found in very dense coastal algal blooms (Hansen et al, 2007). Culture pH ranged daily between pH 8.4 and 8.9 as previously described (Eisensamer and Roenneberg, 2004).…”

Circadian rhythmicity during prolonged chemostat cultivation of Neurospora crassa

“…Indeed the variable periodicity (20 § 4 h) of frq, qrf and ccg-14 mRNA expression and deterioration of periodicity during day 6 and 7 may reXect the loss of feedback cycles between the organism and the medium due to maintenance of constant culture conditions. Nitrogen uptake and metabolism (Christensen et al, 2004;Roenneberg and Rehman, 1996), cellular pH (Eisensamer and Roenneberg, 2004) and redox (Ivleva et al, 2005; and reviewed in Merrow and Roenneberg, 2001), have been reported to Fig. 4.…”