Abstract
Nitric oxide (NO) is a second messenger molecule synthesized by the enzyme nitric oxide synthase (NOS) that requires the molecular chaperone heat shock protein 90 (HSP90) for normal enzymatic activity. Past studies have revealed that both NO and HSP90 act as negative regulators (repressors) of metamorphosis in a diverse range of marine invertebrates, including several molluscan species. Here, we test the role of NO in the metamorphic induction of a vetigastropod mollusc, the tropical abalone Haliotis asinina. Specifically, we 1) test the effects of NO-manipulating pharmacological agents, 2) measure the temporal expression of NOS and HSP90 genes through metamorphosis, and 3) assess the spatial expression of NOS and HSP90 in larvae. We find that inhibition of NOS reduces rates of metamorphosis, indicating that NO facilitates, rather than represses, induction of metamorphosis in H. asinina. The marked increase in NOS expression in putative sensory cells localized to the anterior foot of competent larvae is consistent with NO as an inductive molecule for metamorphosis. In contrast to NOS, HSP90 transcript abundance decreases at competence and there is no evidence of NOS and HSP90 transcript co-localization. This study provides the first evidence of NO as an inductive facilitator of molluscan metamorphosis. Our experimental data suggest that NO modulates signals derived from live inductive substrates via the larval foot to regulate metamorphosis. Inter-specific comparisons of spatial NOS expression in molluscs suggest that the localized pattern of NOS or its protein product is related to the regulatory action of NO in metamorphosis.
Highlights
The ecological success and stability of marine benthic communities depends upon the recruitment of larvae
This allowed us to examine whether application of a pharmacological agent alone is sufficient to induce metamorphosis or sufficient to inhibit the inductive capability of live coralline algae (CA)
We do not believe that our ability to detect an enhanced rate of metamorphosis in the presence of Nitric oxide (NO) donors was constrained by a ceiling effect, because our positive CA controls achieved only 50–70% metamorphosis in these experiments
Summary
The ecological success and stability of marine benthic communities depends upon the recruitment of larvae. These planktonic larvae represent the dispersive phase of a biphasic life cycle that is common among phylogenetically diverse marine invertebrates (Pechenik, 2004; Heyland et al, 2011). To complete the life cycle, free-swimming larvae usually must acquire a state of ontogenic maturation, known as competency (Hadfield et al, 2001), at which time they are able to settle onto an appropriate benthic substrate and undergo metamorphosis into the benthic reproductive form (Hadfield, 1998; Pechenik, 2004). The binding of ligands to their receptors activates conserved biochemical signaling pathways that coordinate the global morphogenetic events that constitute metamorphosis (Hadfield, 2000; Leise and Hadfield, 2000). The application of pharmacological agents that activate or inhibit parts of these conserved signaling pathways can induce settlement and metamorphosis of many species in vitro (Baxter and Morse, 1987; Degnan and Morse, 1995; Biggers and Laufer, 1999; Eri et al, 1999; Amador-Cano et al, 2006)
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