Smith MK et al. (2018), Differences in Small Molecule Neurotransmitter ...

ECB-ART-46718

Front Endocrinol (Lausanne) 2018 Jan 01;9:551. doi: 10.3389/fendo.2018.00551.

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Differences in Small Molecule Neurotransmitter Profiles From the Crown-of-Thorns Seastar Radial Nerve Revealed Between Sexes and Following Food-Deprivation.

Smith MK, Bose U, Mita M, Hall MR, Elizur A, Motti CA, Cummins SF.

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Neurotransmitters serve as chemical mediators of cell communication, and are known to have important roles in regulating numerous physiological and metabolic events in eumetazoans. The Crown-of-Thorns Seastar (COTS) is an asteroid echinoderm that has been the focus of numerous ecological studies due to its negative impact on coral reefs when in large numbers. Research devoted to its neural signaling, from basic anatomy to the key small neurotransmitters, would expand our current understanding of neural-driven biological processes, such as growth and reproduction, and offers a new approach to exploring the propensity for COTS population explosions and subsequent collapse. In this study we investigated the metabolomic profiles of small molecule neurotransmitters in the COTS radial nerve cord. Multivariate analysis shows differential abundance of small molecule neurotransmitters in male and female COTS, and in food-deprived individuals with significant differences between sexes in gamma-aminobutyric acid (GABA), histamine and serotonin, and significant differences in histamine and serotonin between satiation states. Annotation established that the majority of biosynthesis enzyme genes are present in the COTS genome. The spatial distribution of GABA, histamine and serotonin in the radial nerve cord was subsequently confirmed by immunolocalization; serotonin is most prominent within the ectoneural regions, including unique neural bulbs, while GABA and histamine localize primarily within neuropil fibers. Glutamic acid, which was also found in high relative abundance and is a precursor of GABA, is known as a spawning inhibitor in seastars, and as such was tested for inhibition of ovulation ex-vivo which resulted in complete inhibition of oocyte maturation and ovulation induced by 1-Methyladenine. These findings not only advance our knowledge of echinoderm neural signaling processes but also identify potential targets for developing novel approaches for COTS biocontrol.

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Genes referenced: impact LOC100888622 LOC115919910 LOC115925415 LOC575641

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	Figure 1. Untargeted metabolomics analysis of Crown-of-Thorns Seastar radial nerve cord (RNC). (A) Whole-mount micrograph showing location of the COTS RNC. (B) OPLS-DA scores plot, predictive component, t(1), versus orthogonal component, t0(1), showing the supervised separation between the four sample classes. The ellipse represents the Hotelling's T2 95% confidence interval for the multivariate data. (C) Dendrogram displaying the results of the Hierarchical Clustering Analysis (HCA). The plot shows the number of clusters as a function of the vertical coordinate.
	Figure 2. Identification of GABA in the Crown-of-Thorns Seastar. (A) Schematic showing GABA biosynthetic pathway, including enzyme structural organization, domains and mass spectrum for GABA (m/z 126.0654). See File S1 for gene ID and protein sequences for enzymes. (B) Effect of L-glutamic acid on 1-MeAde induced spawning in Crown-of-Thorns Seastar ovarian fragments. (+ + +) Ovulation occurred completely; (++) ovulation occurred, but less than half oocytes remained within the ovary; (+) ovulation occurred partially; and (â€“) no ovulation occurred. Symbols and bars represent the mean for four independent samples and SEM, respectively. (C) Graph showing tentative identification and abundance (mean + SD) of GABA and its derivatives in the radial nerve cord. Significant differences of p < 0.05 are denoted as - a, between control and food-deprived in male; b, between control and food-deprived in female; and c, between male and female COTS. Abundance = the total volume (m/z x retention time x abundance) of the ions associated with this compound.
	Figure 3. Identification of histamine in the Crown-of-Thorns Seastar. (A) Schematic showing histamine biosynthetic pathway, including enzyme structural organization, domains and mass spectrum for histamine (m/z 112.0772). See File S1 for gene ID and protein sequences for enzymes. (B) Graph showing tentative identification and abundance (mean + SD) of histamine from histidine in the radial nerve cord. Significant differences of p < 0.05 are denoted asâ€”a, between control and food-deprived in male; b, between control and food-deprived in female; and c, between male and female COTS. Abundance = the total volume (m/z x retention time x abundance) of the ions associated with this compound.
	Figure 4. Identification of serotonin and melatonin in the Crown-of-Thorns Seastar. Schematic showing (A) serotonin and (B) melatonin biosynthetic pathways, including enzyme structural organization, domains and mass spectrum for serotonin (m/z 177.1329) and melatonin (m/z 233.1588). See File S1 for gene ID and protein sequences for enzymes. (C) Graph showing tentative identification and abundance (mean + SD) of serotonin, melatonin and their derivatives in the radial nerve cord. Significant differences of p < 0.05 are denoted asâ€”a, between control and food-deprived in male; b, between control and food-deprived in female; and c, between male and female COTS. Abundance = the total volume (m/z x retention time x abundance) of the ions associated with this compound.

	Figure 6. Identification of epinephrine and octopamine in the Crown-of-Thorns Seastar. (A) Schematic showing biosynthetic pathway, including enzyme structural organization, domains and mass spectrum for epinephrine (m/z 166.0865). A red X indicates the component was not identified. See File S1 for gene ID and protein sequences for enzymes. (B) Graph showing tentative identification and abundance (mean + SD) of norepinephrine and epinephrine in the radial nerve cord. Significant differences of p<0.05 are denoted as - b, between control and food-deprived in female; and c, between male and female COTS. Abundance = the total volume (m/z x retention time x abundance) of the ions associated with this compound.
	Figure 7. Graph showing tentative identification and abundance (mean + SD) of prostaglandins and their derivatives in the Crown-of-Thorns Seastar radial nerve cord. Significant differences of p < 0.05 are denoted asâ€”a, between control and food-deprived in male; b, between control and food-deprived in female; and c, between male and female COTS. Abundance = the total volume (m/z x retention time x abundance) of the ions associated with this compound.

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Bose, Global metabolite analysis of the land snail Theba pisana hemolymph during active and aestivated states. 2016, Pubmed