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Keywords:

  • chlorophyll fluorescence;
  • enzymes;
  • heat stress;
  • kelp;
  • Laminaria saccharina;
  • nitrogen;
  • photosynthesis;
  • photosystem II;
  • RUBISCO;
  • temperature

ABSTRACT

Mechanisms of high-temperature tolerance in the kelp Laminaria saccharina (L.) Lamour. were examined by comparing a heat-tolerant ecotype from Long Island Sound (LIS), New York, and a population from the Atlantic (ATL) coast of Maine. Greater heat tolerance was not attributable to greater thermal stability of the photosynthetic apparatus: LIS and ATL plants exhibited similar short-term effects of high temperature on photosynthetic capacity (Pmax) and quantum yield (estimated as the ratio of variable to maximum chlorophyll fluorescence, Fv/Fm. As LIS plants had consistently higher N and protein content than ATL plants, the interaction between nitrogen nutrition and high-temperature tolerance was examined. When grown under high N supply and optimal temperature (12° C), LIS plants had a higher density of photosystem II reaction centers (RCII), higher activity of two Calvin cycle enzymes (ribulose bisphosphate carboxylase oxygenase [RUBISCO] and NADP-dependent glyceraldehyde-3-phosphate dehydrogenase [G3PDH]), and higher Pmax and Fv/Fm than ATL plants. Individual ATL plants, furthermore, exhibited close correlations of RCII density and enzyme activity with N and/or protein content. Variation in RCII density and enzyme activity, in turn, largely accounted for plant-to-plant differences in Pmax and Fv/Fm. Relationships among these parameters were generally weak or lacking among individual LIS plants grown under optimal conditions, apparently because luxury N consumption resulted in excess reserves of photosynthetic apparatus components. Exposure of N-replete LIS and ATL plants to a superoptimal temperature (22° C) for 4 days caused an increase in the minimum turnover time of the photosynthetic apparatus (tau) and a decrease in Pmax, but had no consistent effect on Fv/Fm RCII density, PSU size (chlorophyll a/RCII), or enzyme activities. When plants were subjected to concurrent N limitation and heat stress, however, LIS and ATL populations exhibited quite different responses. All photosynthetic parameters of N-limited ATL plants declined sharply in response to high temperature, resulting in a negative rate of daily net C fixation. In contrast, LIS plants showed a reduction in PSU size, but maintained other parameters, including daily C fixation, at levels similar to those of N-limited plants at optimal temperature. Overall, the ability of LIS plants to accumulate and maintain high N reserves appears to be critical for heat tolerance and, therefore, for survival during summer periods of simultaneous low N supply and superoptimal temperature. ATL plants, which also experience low summer N supply but not superoptimal temperatures, do not accumulate large reserves of nitrogenous components and are unable to tolerate the combined stress. Because low N supply often co-occurs with high temperatures in temperate marine systems, large-scale declines in algal productivity, such as during El Niño events, are probably due to the interactive effect of N limitation and heat stress.