Acid lysis of macroalgae by marine herbivorous fishes: effects of acid pH on cell wall porosity

Abstract

It has been demonstrated that treatment of algae at low pH values, similar to those found in the stomachs of herbivorous fishes, damages the algal cells, allowing digestive enzymes to enter the cells. However, the effects of the low pH treatment on the porosity of algal cell walls has not been examined. We tested the effects of low pH on the porosity of cells of four species of dietary algae, Enteromorpha intestinalis and Ulva rigida (Chlorophyta) and Porphyra sp. and Polysiphonia strictissima (Rhodophyta) consumed by herbivorous fishes. The uptake of fluorescein isothiocyanate (FITC)-conjugated dextrans of different molecular sizes was used to determine the cell-wall pore size in these algae. Secondly we tested whether acidic conditions increased the porosity of the algal cell walls by first immersing the algae in seawater adjusted to a low pH, then used the uptake of the FITC-dextrans into the acid treated cells to measure changes in cell-wall porosity. Limiting cell-wall pore diameter in E. intestinalis, U. rigida and P. strictissima was less than 8.8 nm, and in Porphyra sp. was less than 7.1 nm. The low pH treatment increased the porosity of the cell walls in all four algae. Porphyra sp. was the most resistant to this low pH treatment, followed by P. strictissima, then E. intestinalis and finally U. rigida. The cell-wall pore size of all algae increased to at least 13.5 nm after 20 min at pH 2.0, and after 60 min at either pH 2.5 or pH 3.0. These findings have important implications for the ability of marine herbivorous fish to digest these algae. Fish proteases range in molecular diameter from 4.2 to 5.4 nm and would therefore be able to pass through the cell walls of untreated algae in under 10 min. α-Amylases have molecular diameters ranging from 6.1 to 6.5 nm, and would require up to 30 min to traverse the algal cell walls. The increase in algal cell-wall porosity as a result of exposure to low pH conditions in the stomachs of marine herbivorous fishes would allow molecules, similar in size to proteases and α-amylases, to enter the cells in under 5 min, and is therefore likely to be an important factor in the digestion of intracellular algal nutrients.