GABA is an inhibitory neurotransmitter in the neural circuit regulating metamorphosis in a marine snail

Abstract

The marine mud snail, Tritia (=Ilyanassa) obsoleta, displays a biphasic life cycle. During the initial phase of early development, embryos hatch from benthic egg capsules to become weakly swimming veliger larvae. In the second phase, adult T. obsoleta are facultative carnivores and major agents of community disturbance. Metamorphosis is the irreversible developmental event that links these two life history stages. When physiologically competent, larvae can respond to appropriate environmental cues by settling onto their mudflat habitat and transforming themselves into miniature adult snails. Two neurotransmitters-serotonin and nitric oxide-have opposing effects on the metamorphic process in this species. In multiple other species of gastropod and bivalve molluscs, a third neurotransmitter, the classically inhibitory compound γ-aminobutyric acid (GABA), can induce settlement or metamorphosis upon external application to competent larvae. In this situation, GABA is presumed to mimic the action of ligands from the juvenile environment that bind to larval chemosensory receptors and activate the metamorphic pathway. Results of our experiments contradict this commonly reported action of GABA on molluscan larvae. External application of GABA to competent larvae of T. obsoleta elicited no response, but instead attenuated the action of serotonin (5-HT), a metamorphic inducer. Our investigations into the responses of larval T. obsoleta to multiple GABAergic reagents support our hypothesis that GABA functions internally as a neurotransmitter in the pathway that controls the initiation of metamorphosis. Our results also suggest that GABA acts directly on or downstream from serotonergic neurons to regulate the metamorphosis-inducing effects of this neurotransmitter. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 736-753, 2018.

Toward a Mechanistic Understanding of Marine Invertebrate Behavior at Elevated CO2

“…iGABA R signaling mediates swimming of larval sea urchins (Katow et al, 2013), the righting response in a sea urchin (Shelley et al, 2019) and locomotion of a mollusk (Romanova et al, 1996). GABA mediates settling and metamorphosis, including associated behavioral changes in a range of mollusks (Morse et al, 1979;Morse et al, 1980;García-Lavandeira et al, 2005;Stewart et al, 2011;Biscocho et al, 2018), an echinoderm (Pearce and Scheibling, 1990) and a urochordate (Danqing et al, 2006). GABA is thought to mimic ligands from the environment (Morse et al, 1979) which may be detected by the iGABA R (Stewart et al, 2011) to initiate settlement and metamorphosis.…”

“…GABA is thought to mimic ligands from the environment (Morse et al, 1979) which may be detected by the iGABA R (Stewart et al, 2011) to initiate settlement and metamorphosis. Internal iGABA R mediated neurotransmission is also suggested to regulate metamorphosis (Biscocho et al, 2018). Thus altered iGABA R function will likely affect a variety of behaviors in a range of marine invertebrates.…”

Tetrabromobisphenol A acts a neurodevelopmental disruptor in early larval stages of Mytilus galloprovincialis

“…2019;Smart and Stephenson, 2019): in molluscs, GABA has been shown to affect larval settlement and metamorphosis, with possible downstream effects on serotonin pathways(Biscocho et al, 2018; Joyce and Vogeler, 2018, and refs therein). The high abundance of GABA-ir cells observed in control mussel trocophorae (at 24 hpf) is in line with the role of this neurotransmitter in the early developing mammalian brain, where the GABAergic system plays an important trophic role, even prior to synaptogenesis, in the proliferation of neuronal progenitor cells (reviewed inWu and Sun, 2016).…”

Signaling via GABAB receptors regulates early development and neurogenesis in the basal metazoan Nematostella vectensis

“…This effect was reversible and showed no toxicity, while removal of GABABR modulators led to a continuation of the Nematostella developmental plan. Interestingly, in other marine invertebrate such as molluscs and sea urchins, GABA was suggested to play a role in metamorphosis, either as an inducer or as an inhibitor, but receptors mediating these effects have not been characterized nor additional GABA signaling components have been implicated (48)(49)(50). In contrast, our characterization of putative Nematostella GABABR homologs identified four genes with all the conserved features of a functional GABAB1R.…”