SULFIDE DETOXIFICATION AND TOLERANCE IN HALICRYPTUS-SPINULOSUS (PRIAPULIDA) - A MULTIPLE STRATEGY

The detoxification potential of Halicryptus spinulosus in the presence of sulfide was studied. The worms are able to cope with considerable amounts of sulfide. They benefit from several survival strategies for controlling sulfide dose and detoxifying sulfide that enters the body. When oxygen and sulfide occur concurrently in the environment sulfide can either initially be excluded or internal concentration kept low by the animals. Non-toxic thiosulfate, the main detoxification product, accumulates up to 3856 +/- 997 muM in the hemolymph. Sulfide has an overriding influence on the aerobic metabolism and imposes anaerobiosis even though oxygen is available, i.e. sulfide-induced anaerobiosis. Succinate, an indicator of anaerobic metabolism, accumulates during persistent oxic sulfide incubation to 12.3 +/- 2.3 mumol ml-1 in hemolymph and to 3.0 +/- 1.3 mumol g-1 fresh mass in body wall after 10 d. During anoxic sulfide exposure, the animals make use of graded strategies. Some sulfide is immobilised in an external barrier due to iron-sulfide formation. The iron-sulfide compound results in a conspicuous blackening of the animal and its blood. This blackening is fully reversible upon receiving oxygen again. Detoxification to thiosulfate, depending on the oxygen storage capacity of the hemolymph, amounted to only a minor level, with a maximum of 172 +/- 49 muM in the hemolymph after 1 d of incubation. Sulfide also binds to a presently unknown hemolymphic factor. This binding may temporarily protect mitochondria, a main location of sulfide detoxification. The mitochondrial enzyme for aerobic metabolism, cytochrome c oxidase, is inhibited by low sulfide levels in vitro (K(i) 1.05 +/- 0.22 muM), and has a much higher in vivo resistance in whole animals. Catalase, another sulfide sensitive enzyme, has a K(i) of ca 200 muM in vitro and is unaffected in vivo. Internal sulfide concentration in the hemolymph increases ca 3-fold (570 +/- 298 muM) over external levels during long-term exposure experiments with 200 muM sulfide. The survival in spite of such an elevated amount of internal sulfide accumulation is unprecedented for a marine invertebrate without endosymbionts. The worms can passively outlast raised environmental sulfide concentrations by their high capacity for anaerobic metabolism.