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Nitric Oxide Inhibits Metamorphosis in Larvae of Crepidula fornicata, the Slippershell Snail

¹ Biology Department, Tufts University, Medford, Massachusetts 02155
² Biology Department, Dickinson College, Carlisle, Pennsylvania 17013

^* To whom correspondence should be addressed. E-mail: jan.pechenik{at}tufts.edu

This paper concerns the role of nitric oxide (NO) in controlling metamorphosis in the marine gastropod Crepidula fornicata. Metamorphosis was stimulated by the nitric oxide synthase (NOS) inhibitors AGH (aminoguanidine hemisulfate) and SMIS (S-methylisothiourea sulfate) at concentrations of about 100–1000 µmol l^–1 and 50–200 µmol l^–1, respectively. Metamorphosis was not, however, induced by the NOS inhibitor L-NAME (L-N^G-nitroarginine methyl ester) at even the highest concentration tested, 500 µmol l^–1. Moreover, pre-incubation with L-NAME at 20 and 80 µmol l^–1 did not increase the sensitivity of competent larvae to excess K⁺, a potent inducer of metamorphosis in this species; we suggest that either L-NAME is ineffective in suppressing NO production in larvae of C. fornicata, or that it works only on the constitutive isoform of the enzyme. In contrast, metamorphosis was potentiated by the guanylate cyclase inhibitor ODQ (1H-[1,2,4]oxadiazolo[4,3, -a]quinoxalin-1-one) in response to a natural metamorphic inducer derived from conspecific adults. Because NO typically stimulates cGMP production through the activation of soluble guanylate cyclase, this result supports the hypothesis that NO acts as an endogenous inhibitor of metamorphosis in C. fornicata. The expression of NOS, shown by immunohistochemical techniques, was detected in the apical ganglion of young larvae but not in older larvae, further supporting the hypothesis that metamorphosis in C. fornicata is made possible by declines in the endogenous concentration of NO during development.

Abbreviations: ACSW, adult-conditioned seawater • AGH, aminoguanidine hemisulfate • FSW, filtered seawater • IO, instant ocean artificial seawater • L-NAME, L-N^G-nitroarginine methyl ester • LTC, L-thiocitrulline • NO, nitric oxide • NOS, nitric oxide synthase • NOS-LIR, NOS-like immunoreactivity • ODQ, 1H-[1,2,4]oxadiazolo[4,3,-a]quinoxalin-1-one • SMIS, S-methylisothiourea sulfate