Photosynthetic and behavioral versatility of the cyanobacterium Oscillatoira boryana in a sulfide-rich microbial mat

Abstract

The diel pattern of vertical migratory movements and photosynthetic activity of Oscillatoria cf. boryana was monitored periodically in microbial mats of a shallow tepid pond fed by sulfiderich, hot, geothermal spring water in Rotorua, New Zealand. Motile O. boryana formed a conspicuous and predominant population which was spread over the mat surface during darkness and on overcast days (< 50–100 W m−2). Macrophotography has documented that under higher light (100–300 W m −2) much of the population contracted into streaks or patches. During periods of even higher irradiance (>300 W m−2), O. boryarta disap-peared almost entirely from the mat surface to a position of about 1 mm below the surface pellicle of the mat. O2, sulfide, and pH microelectrodes inserted into excised mat cores with dense O. boryana populations were used to make vertical profiles at intervals of 0.1−0.2 mm and also to estimate rates of oxygenic and anoxygenic photosynthesis during rapid light-dark transitions. In addition, attenuation of irraaiance was measured in mats with O. boryana by a spectroradiometer with mini-fiber optic probe. Light-dependent incorporation of [ 14C]-bicarbonate and [14C]-acetate was measured in collected field populations of O. boryana. The combined results led to the conclusion that populations of O. boryarta typically employed sulfide-dependent anoxTgenic photosynthesis in early morning which depleted sulfide locally. As irradiance increased and sulfide concentration fell below about 50 µM within the Oscillatoria population, oxygenic photosynthesis became dominant. [14C]-Bicarbonate incorporation results indicate that sulfide concentrations over 1.0 mM inhibit oxygenic photosynthesis completely. In populations on excised mats, irradiance levels of about 150–200 W m −2 were required for light-enhanced oxidation of sulfide to balance sulfide input from diffusion and local production. Below that surface-irradiance level it is likely that mainly sulfide-dependent anoxygenic photosynthesis of O. boryana occurred. This capability was confirmed for O. boryana by [14C]-photoincorporation and sulfide-microeleetrode experiments. Forced exposure to high irradiance levels (500–700 W m −2) was inhibitory to oxygenic photosynthesis in O. boryana, but these intensities impinging on mats resulted in a downward retreat. The result was a lowered irradiance level for the Oscillatoria but, nevertheless, a high rate of oxygenic photosynthesis. O. boryana is a versatile cyanobacterium that appears to avoid photoinhibitory conditions and to optimize its light intensity for photosynthesis by vertical migrations, using gliding motility and some form of photoresponse. It is also able to photosynthesize at substantial rates over a wide range of sulfide concentrations by shifting between oxygenic and anoxygenic modes or possibly by combining both.