Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage

Abstract

Activated defenses against herbivores and predators are defenses whereby a precursor compound is stored in an inactive or mildly active form. Upon damage to the prey, the precursor is enzymatically converted to a more potent toxin or feeding deterrent. In marine systems, activated defenses are only known to exist in a few species of tropical macroalgae. In this study, we examined an activated defense system in temperate marine macroalgae in which the osmolyte dimethylsulfo- niopropionate (DMSP) is converted to acrylic acid or acrylate, depending upon the pH, and dimethyl sulfide (DMS) by the enzyme DMSP lyase upon damage to the alga. We surveyed 39 species of red, green, and brown algae from the Washington and Oregon coasts, and found high concentrations of DMSP in the chlorophytes Acrosiphonia coalita, Codium fragile, Enteromorpha intestinalis, E. linza, Ulva californica, U. fenestrata, and U. taeniata, and in the rhodophyte Polysiphonia hendryi. Con- centrations of DMSP ranged from 0.04% of the alga's fresh mass (FM) to 1.8% FM. We found signif- icant DMSP lyase activity in 1 green alga, U. fenestrata, and 1 red alga, P. hendryi, with DMSP cleav- age rates approaching 300 mmol kg -1 FM min -1 . Loss of DMSP and the production of DMS when the tissues of U. californica and P. hendryi were crushed suggested that physical damage results in DMSP cleavage. In laboratory feeding preference experiments, acrylic acid deterred feeding by the sea urchin Strongylocentrotus droebachiensis at concentrations of 0.1 to 2% FM and by S. purpura- tus at 0.25 to 2% FM, while the precursor DMSP functioned as a feeding attractant to both sea urchins. In contrast, feeding by the isopod Idotea wosnesenskii was not deterred by acrylic acid even at concentrations as high as 8% FM. Our data suggest that DMSP may function as a precursor in an activated defense system in diverse species of temperate macroalgae and may possibly contribute to the widespread success of the Ulvophyceae. This chemical system is also found in unicellular phyto- plankton, and presents an opportunity to compare and contrast the ecological role of chemical defense among micro- and macroorganisms.