Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency

Summary

Ten species of brown macroalgae (five eulittoral and one submersed species of the Fucales; four submersed species of the Laminariales) from a rocky shore at Arbroath, Scotland, were examined for characteristics of emersed photosynthesis in relation to the partial pressure of CO₂ and O₂. The five eulittoral species of the Fucaceae were approaching CO₂ saturation for light-saturated photosynthesis at normal air levels of CO₂ (35 Pa) in 21 kPa O₂. The normally submersed algae are further from CO₂ saturation under these conditions, especially in the case of the four members of the Laminariales. The rate of net photosynthesis in the Fucaceae is O₂-independent in the range 2–21 kPa O₂ over the entire range of CO₂ partial pressure tested (compensation up to 95 Pa). For the other five algae tested, net photosynthesis is slightly inhibited by O₂ at 21 kPa relative to 2 kPa over the entire range of CO₂ partial pressures tested (compensation up to 95 Pa). CO₂ compensation partial pressures are low (<0.5 Pa) for the Fucaceae and independent of O₂ in the range 2–42 kPa. For the other five algae, the CO₂ compensation partial pressure are higher, and increased with O₂ partial pressure in the range 2–42 kPa. These gas exchange data show that the Fucaceae exhibit more C₄-like characteristics of their photosynthetic physiology than do the other five species tested, although even the Laminariales and Halidrys siliquosa are not classic C₃ plants in their photosynthetic physiology. These data suggest that, in emersed conditions as well as in the previously reported work on submersed photosynthesis, a “CO₂ concentrating mechanism” is operating which, by energized transmembrane transport of inorganic C, accumulates CO₂ at the site of RUBISCO and, at least in part, suppresses the oxygenase activity. Work with added extracellular carbonic anhydrase (CA), and with a relatively membrane-impermeant inhibitor of the native extracellular CA activity (acetazolamide), suggests that, in emersed conditions as well as in the previously reported work on algae submersed in seawater at pH 8, HCO ^sup−_inf3 is the major inorganic C species entering the cell. At optimal hydration, the rate of emersed photosynthesis in air is not less than the rate of photosynthesis when submersed in seawater, at least for the Fucaceae. δ¹³C ratios of organic C for the Fucaceae are slightly more negative than is the case for the other five algae; these data are consitent with substantial (half or more of the entering inorganic C) leakage of CO₂ from the accumulated pool, and with some contribution of atmospheric CO₂ to the organic C gain by the eulittoral algae. The predicted increase in N use efficiency of photosynthesis in the Fucaceae, with their more strongly developed CO₂ concentrating mechanism, is consistent with data on emersed, but not submersed, photosynthesis for the algae collected from the wild and thus at a poorly defined N status. The more C₄-like gas exchange charateristics of photosynthesis in the eulittoral Fucaceae may be important in increasing the water use efficiency of emersed photosynthesis from the limited capital of water available for transpiration by a haptophyte.