Effects of Visible Light and UV Radiation on Photosynthesis in a Population of a Hot Spring Cyanobacterium, a Synechococcus sp., Subjected to High-Temperature Stress

Unicellular cyanobacteria formerly assigned to the morphospecies Synechococcus cf. lividus Copeland are major components of microbial mat communities in alkaline hot springs of the Western hemisphere and East Asia at temperatures ranging from approximately 45 to 73°C, the upper temperature limit of photosynthetic life (2, 6, 7). It is the only cyanobacterial morphospecies found above 64°C. Early studies in laboratory culture of clones isolated from an Oregon hot spring have provided evidence for the existence of multiple strains of this morphospecies that vary in optimal growth temperature and growth temperature range (31), and recent investigations suggest that these temperature strains may have diverged at the 16S rRNA sequence level (11, 28). The effects of temperature on photosynthesis and growth of oxygenic phototrophs have been well described (8, 10). Reduction in photosynthesis at supraoptimal but nonlethal temperature is the product of both increased photorespiration as a result of higher affinity of ribulose-1,5-bisphosphate carboxylase/oxygenase (RUBISCO) for O2 with increasing temperature and lowered activity of RUBISCO and/or its activase (8, 10, 21). The lethal temperature has been found in plants and algae to be determined by the thermal stability of the thylakoid membrane, of which photosystem II is the most labile component (10). Suboptimal temperature effects on photosynthesis include rate limitation by enzymatic reactions due to thermodynamic constraints, limitation for inorganic phosphate, and feedback inhibition resulting from accumulation of photosynthetic end products (10). The question of whether populations of Synechococcus sp. growing at the upper limit of their range are optimally adapted to local means or extremes in their thermal environment has not been resolved by previous studies. After investigating inorganic carbon fixation by a Synechococcus sp. collected from different temperatures along the outflow of Mushroom Spring, Lower Geyser Basin, Yellowstone National Park, T. D. Brock and M. L. Brock (2–4) reported a positive relationship between the mean temperature of collection and the optimal temperature for photosynthesis. It was concluded that populations of these cyanobacteria have evolved such that their optimal temperature for growth and photosynthesis matches mean environmental temperature, even at 70°C, near the upper limit of their range. Data obtained in laboratory culture, however, indicate that optimal temperature for both growth and photosynthesis of a clone isolated from a sample collected near the upper temperature limit from Hunter’s Hot Springs, Oreg., ranges from 63 to 67°C, lower than the mean environmental temperature of >70°C (25). These laboratory results suggest that these bacteria are subjected to chronic temperature stress in nature. Resolution of this issue has implications for our understanding of the limits of physiological tolerance and adaptation in these bacteria. In order to determine whether a population of Synechococcus sp. from Octopus Spring, Lower Geyser Basin, Yellowstone National Park, which was growing near the upper temperature limit for photosynthetic life, was optimally adapted photosynthetically to its local thermal environment, photosynthesis was measured during the summers of 1995 and 1996 at three temperatures: 70, 65, and 55°C. The first was the approximate mean temperature of the environment, and these temperature treatments were hypothesized to be supraoptimal, optimal, and suboptimal for photosynthesis, respectively, based on the laboratory culture data of Meeks and Castenholz (25). Cells were simultaneously exposed to modified solar environments, including reduction of total irradiance and exclusion of UV radiation, in order to investigate whether and how temperature-dependent effects on photosynthetic uptake interact with these factors (e.g., whether effects of nonoptimal temperature are exacerbated with increasing irradiance). In addition, we evaluated whether the Octopus Spring high-temperature Synechococcus sp. was subject to diurnal inhibition of photosynthesis and whether inhibition, if observed, had a UV radiation component.