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

Activated defenses against herbivores and predators are defenses whereby a precursor compound is stored in an inactive or mildly active form. Upon dam age 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 e xamined an activated defense system in temperate marine macroalgae in which the osmolyte dimethylsulfoniopropionate (DMSP) is converted to acrylic aci d or acrylate, depending upon the pH, and dimethyl sulfide (DMS) by the enz yme DMSP lyase upon damage to the alga. We surveyed 39 species of red, gree n, and brown algae from the Washington and Oregon coasts, and found high co ncentrations of DMSP in the chlorophytes Acrosiphonia coalita, Codium fragi le, Enteromorpha intestinalis, E. linza, Ulva californica, U. fenestrata, a nd U, taeniata, and in the rhodophyte Polysiphonia hendryi. Concentrations of DMSP ranged from 0.04 % of the alga's fresh mass (FM) to 1.8 % FM. We fo und significant DMSP lyase activity in 1 green alga, U. fenestrata, and 1 r ed alga, P, hendryi, with DMSP cleavage rates approaching 300 mmol kg(-1) F M min(-1). Loss of DMSP and the production of DMS when the tissues of U. ca lifornica and P, hendryi were crushed suggested that physical. damage resul ts in DMSP cleavage. In laboratory feeding preference experiments, acrylic acid deterred feeding by the sea urchin Strongylocentrotus droebachiensis a t concentrations of 0.1 to 2 % FM and by S. pupuratus at 0.25 to 2% FM, whi le the precursor DMSP functioned as a feeding attractant to both sea urchin s. In contrast, feeding by the isopod Idotea wosnesenskii was not deterred by acrylic acid even at concentrations as high as 1.8 % FM. Our data sugges t that DMSP may function as a precursor in an activated defense system in d iverse species of temperate macroalgae and may possibly contribute to the w idespread success of the Ulvophyceae. This chemical system is also found in unicellular phytoplankton, and presents an opportunity to compare and cont rast the ecological role of chemical defense among micro- and macroorganism s.