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Photosynthetic rhythmicity in an antarctic microbial mat and some considerations on polar circadian rhythms

CHARLES S. COCKELL, Carnegie Institute of Washington, Stanford, California 94305-1297

LYNN J. ROTHSCHILD, Ecosystem Science and Technology Branch, National Aeronautics and Space Administration, Ames Research Center, Moffett Field, California 94035-1000

Many physiological processes in organisms, particularly photosynthesis, exhibit diurnal patterns (e.g., Hoffman and Dawes 1980; Rothschild 1991; Stock and Ward 1991). The light/dark cycle that all organisms above the Antarctic Circle (66°S) experience allows related physiological processes to become entrained in a circadian fashion, for example, amino-acid uptake, enzyme levels, and the onset of mitosis. Continuous light is often found to result in a disruption of entrainment (e.g., Chen et al. 1991; Makarov, Schoschina, and Luning 1995). At the poles, photosynthetic organisms are subjected to a 24-hour light cycle during the summer, without a dark period. Diurnal light intensity approaches near continuous at 90°S. Here, data from a simple study of the diurnal photosynthetic pattern in an Oscillatoria mat from Bratina Island are shown. Associated thoughts on possible research directions on natural photosynthetically driven polar cycles are made.

Experimental procedures and results

The mat studied was collected from Skua Pond, Bratina Island, part of the McMurdo shelf ablation zone (78°S 166°E). Mats from this pond have been described previously (Vincent et al. 1993) and are composed primarily of the filamentous cyanobacteria Oscillatoria . Cores of mat of size 1.9 square centimeters were collected in water from Skua Pond and returned to McMurdo Station (78°15'S 166°30'E), which had the same light cycle as Bratina. Mats were maintained in trays at a water depth similar to that found in the field (5 centimeters). The following day, carbon fixation was studied using carbon-14-bicarbonate using a modification of Goldman (1963) and as described in Rothschild (1991). Three cores were placed in separate whirlpak bags, and 10 microcuries per milliliter of carbon-14-bicarbonate (New England Nuclear, Wilmington, Delaware, catalog number NEC 086H) were added to 3 milliliters of Skua Pond water in the bags with a final concentration of 102 microcuries per milliliter. The mats were incubated for 2 hours under natural light and frozen on dry ice. Five milliliters of 0.5 molar Tris pH 7.5 were added to each bag and cores were sonicated until a homogenate had been formed. Two-hundred microliters of homogenate was removed and added to 100 microliters of acetic acid in a scintillation vial. Samples were air dried and counted. Results are plotted as the mean of the triplicates against time of day (figure). Results are plotted as disintegrations per minute per hour of incubation since the dissolved inorganic carbon concentration of the Skua Pond water is not known. Standard deviations were no more than 5 percent of each point. At each time point, a dark control was run (a sample covered in silver foil). The temperature of the mats remained at 5°C, ambient air temperature, throughout the experiment. Light measurements were taken every 2 hours using a LiCor Model L-189 light meter (LiCor, Lincoln, Nebraska). Chlorophyll was extracted with methanol and concentrations calculated using the equations of Lorenzen (1967). Chlorophyll- a concentrations were an average of 13.4 micrograms of chlorophyll- a per square centimeter, similar to previous observations on antarctic freshwater Oscillatoracean mats (Vincent et al. 1993).

Discussion

Organisms below the Antarctic Circle (66°S) and in the corresponding Arctic regions, experience a 24-hour light cycle during the photosynthetically active summer period, but one that has varying intensity and magnitude of variation depending on latitude. In this study, a simple examination of the summer photosynthetic pattern in a natural Oscillatoria microbial mat from Skua Pond, Bratina Island, Antarctica, was made.

At McMurdo Station, an order of magnitude difference in photosynthetically available radiation between midnight and midday occurs during January. This difference was found to be tracked by the diurnal photosynthetic response. Photosynthesis was not completely shutdown at midnight but instead continued to occur above background similarly for other antarctic microbial communities that have been studied (e.g., Goldman 1972). A midday drop in photosynthesis was not observed in the microbial mat as is observed in temperate mats (Rothschild 1991). This absence of a drop may be due to better photoprotection and probably differing light inhibition levels of antarctic organisms.

Other ecological factors such as temperature may determine diurnal response of mats in different areas of Antarctica, and so response to irradiance may not necessarily be a simple correlation. Diurnal photosynthetic changes in such communities, however, raise interesting questions on polar circadian rhythms.

Photosynthetic organisms that approach 90°S, such as the lichens in the Horlick Mountains (86°S) (Wise and Gressitt 1965), will experience less diurnal rhythmicity in light intensity since light approaches continuous nearer 90°S. Such organisms would be an interesting target of study for research on polar circadian cycles since continuous nonvarying light cycles result in the disruption or change of rhythms in many organisms (e.g., Chen et al. 1991; Makarov et al. 1995). Future research might also concentrate on studying the continuity of physiological rhythms after light has been shut off. Such a study would allow for the examination of entrainment and how rhythms are regulated in natural photosynthetic communities exposed to near continuous light.

Acknowledgments

This work was supported by National Science Foundation grant OPP 93-17696 to the University of Southern California. Acknowledgments are made to Tracie Nadeau, Antonio Quesada, Rodney Forster, and Mariana de Oliveira for their assistance in this work at McMurdo, and Donal Manahan for course organization.

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