Bicarbonate uptake and utilization in marine macroalgae

Abstract

Several macroalgae from the Swedish West Coast (11 green, 5 red and 11 brown algal species) and two Ulva spp. from the Mediterranean were tested for mechanisms of HCO₃⁻ utilization. In all except one (Palmaria palmata), photosynthesis supported by inorganic carbon (Ci) at pH 8.7 was rapidly and substantially (>50%) inhibited by acetazolamide (AZ), an inhibitor of extracellular carbonic anhydrase activity. This suggests that extracellular dehydration followed by uptake of the CO₂ formed is an important component of the HCO₃⁻ utilization mechanism(s) of these algae. In representatives of most of the green algal genera, e.g. Enteromorpha, Ulva, Chaetomorpha and Monostroma, a specific inhibitor response could be induced. This response, a sensitivity to the anion exchange inhibitor 4,4′-diisothiocyanatostilbene-2,2′-disulphonate (DIDS) in the presence of AZ, is characteristic of an additional mechanism of HCO₃⁻ utilization, a direct import of HCO₃⁻ across the plasma membrane, which has been previously described only for some Ulva spp. and Enteromorpha intestinalis. The DIDS sensitivity could be induced in several ways, all involving a potential shortage of the supply of CO₂ for photosynthesis: through photosynthesis at high pH, through growth in strong light and nutrient-rich seawater, or through photosynthesis in the presence of AZ. Induction of photosynthesis at high pH (which is a specific feature of green macroalgae) was not always accompanied by a development of this specific DIDS sensitivity; it occurred in Chaetomorpha melagonium but not in C. linum. For Ulva lactuca cultivated in natural seawater (in continuous moderate irradiance), induction of DIDS sensitivity by high pH treatment was successful all year round, except during a period in late August. The results thus suggest that green macroalgae capable of developing photosynthesis at high pH are also capable of developing a DIDS-sensitive mechanism for HCO₃⁻ uptake, but that some additional conditions (other than low CO₂ availability) must be fulfilled. The ability to dehydrate extracellular HCO₃⁻ still remained after induction of the direct HCO₃⁻ uptake, and the two mechanisms for HCO₃⁻ utilization may operate independently of one another. In fact the response to DIDS was more pronounced after the addition of AZ. The possibility that the results are related to a plasticity of the HCO₃⁻-utilizing mechanisms of green macroalgae is discussed. Neither red nor brown macroalgae showed any sensitivity to DIDS in the presence of AZ.