Ecotoxicity of hallachrome, an unusual 1-2 anthraquinone excreted by the infaunal polychaete Halla parthenopeia: evidence for a chemical defence?

Abstract

Polychaetes play a prominent role in marine systems, but little is known about their secondary metabolites compared with other benthic taxa. In the present study, we investigated the toxicity of hallachrome, an unusual 1-2 anthraquinone identified from the skin of some polychaetes, including the Mediterranean infaunal species Halla parthenopeia. Under stress conditions, this worm releases a harmful purple mucus, whose noxious compounds were still unknown. We hypothesized that hallachrome also occurs in the purple mucus, giving rise to its color and toxicity. Soon after the production of the purple exudate, H. parthenopeia also secretes a harmless, transparent mucus, which pushes away the toxic one, suggesting protective functions for the worm itself. LC-MS and ¹H-NMR analyses confirmed the presence of the pigment hallachrome in the purple mucus. The average concentration of the pigment in the purple mucus was about 310 mg L^-1. Ecotoxicological bioassays on representative species of bacteria, protozoans, rotifers, crustaceans (Artemia franciscana) and polychaetes (Dinophilus gyrociliatus) revealed its severe toxic effects: LC₅₀/EC₅₀ values ranged from 0.11-5.67 mg L^-1. Hallachrome showed higher toxicity for A. franciscana than other naturally occurring anthraquinones. Tests on encapsulated embryos of D. gyrociliatus evidenced the ability of a mucus layer to limit hallachrome diffusion, confirming the protective role of the transparent mucus. Given the information available on polychaetes anti-predator strategies, hallachrome cannot be considered a consumer deterrent. However its toxicity and wide range of activity suggest chemical defensive functions against potential competitors, parasites and/or pathogens.