Abstract
Marine invertebrates undergo distinct life cycles and development processes, and some undergo a metamorphic transition from pelagic larvae to benthic juvenile. Previous studies have shown that the second messenger nitric oxide (NO) plays important roles in regulating larval metamorphosis in marine invertebrates. However, this regulatory function is not conserved. Herein, we investigated the regulatory role of NO in larval metamorphosis in Hard-shelled mussel (Mytilus coruscus). Pharmacological experiments revealed that after exposure to nitric oxide synthase (NOS) inhibitors, the larval metamorphosis rate was increased significantly. By contrast, exposure to NO donors significantly reduced the larval metamorphosis rate. To further investigate the function of NO in metamorphosis, we cloned the NOS cDNA sequence from M. coruscus (McNOS), analyzed amino acid sequences of McNOS from different species, and measured McNOS mRNA temporal expression alongside the molecular chaperone heat shock protein 90 (HSP90) in different larval stages. The results showed that NOS proteins share a highly conserved domain sequence in different species, even in invertebrates and vertebrates, but their classification among invertebrates and vertebrates is not the same. Except for the umbo veliger stage, McNOS mRNA was expressed at low levels in pediveliger larval and post-larvae stage, indicating a potential inhibitory function for NO in larval metamorphosis. Meanwhile, HSP90 mRNA expression was correspondingly high in the umbo veliger stage and lower in the pediveliger larval and post-larvae stage, indicating potential functional synergism. Interestingly, McNOS enzyme activity in different larval stages was inconsistent with its mRNA expression. Metamorphosis assays of pharmacological treatments combined with McNOS and HSP90 gene expression and NOS enzyme activity analyses indicated that NO acts as a suppressor to regulate metamorphosis in M. coruscus, regardless of whether nitric oxide is endogenous or exogenous.
Highlights
Marine invertebrates are major members of coastal and marine benthic communities, and they are characterized by indirect development with a dispersive larval stage in their life histories (Qian, 1999)
Larval settlement and metamorphosis are determined by exogenous factors such as physical, biological, or chemical parameters related to the substratum, derived from conspecific or congeneric individuals, biofilms, sympatric species, food, or habitats, as well as endogenous factors such as the neurotransmitters (Qian, 1999; Joyce and Vogeler, 2018)
In 24-h exposure trials, compared with negative controls (FSW and dimethyl sulfoxide (DMSO)), the metamorphosis rate of larvae was significantly increased after exposure to all tested nitric oxide synthase (NOS) inhibitors (p < 0.05, Figure 1)
Summary
Marine invertebrates are major members of coastal and marine benthic communities, and they are characterized by indirect development with a dispersive larval stage in their life histories (Qian, 1999). Receptors on sensory organs can receive signals from appropriate environmentderived ligands such as biological cues from bacterial biofilms and conspecifics, chemical cues including ion concentrations, ammonia, and neuroactive compounds such as epinephrine (EPI), 5-hydroxytryptamine, L-3,4-dihydroxyphenylalanine, γ-aminobutyric acid, acetylcholine, and isobutyl-methylxanthine (Beiras and Widdows, 1995; García-Lavandeira et al, 2005; Teh et al, 2012; Grant et al, 2013; Mesías-Gansbiller et al, 2013; Joyce and Vogeler, 2018) These signals activate conserved intercellular signaling pathways and thereby regulate settlement and metamorphosis of larvae (Hadfield et al, 2000)
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