The Gastric Ganglion of Octopus vulgaris: Preliminary Characterization of Gene- and Putative Neurochemical-Complexity, and the Effect of Aggregata octopiana Digestive Tract Infection on Gene Expression

Abstract

The gastric ganglion is the largest visceral ganglion in cephalopods. It is connected to the brain and is implicated in regulation of digestive tract functions. Here we have investigated the neurochemical complexity (through in silico gene expression analysis and immunohistochemistry) of the gastric ganglion in Octopus vulgaris and tested whether the expression of a selected number of genes was influenced by the magnitude of digestive tract parasitic infection by Aggregata octopiana. Novel evidence was obtained for putative peptide and non-peptide neurotransmitters in the gastric ganglion: cephalotocin, corticotrophin releasing factor, FMRFamide, gamma amino butyric acid, 5-hydroxytryptamine, molluscan insulin-related peptide 3, peptide PRQFV-amide, and tachykinin–related peptide. Receptors for cholecystokininA and cholecystokininB, and orexin2 were also identified in this context for the first time. We report evidence for acetylcholine, dopamine, noradrenaline, octopamine, small cardioactive peptide related peptide, and receptors for cephalotocin and octopressin, confirming previous publications. The effects of Aggregata observed here extend those previously described by showing effects on the gastric ganglion; in animals with a higher level of infection, genes implicated in inflammation (NFκB, fascin, serpinB10 and the toll-like 3 receptor) increased their relative expression, but TNF-α gene expression was lower as was expression of other genes implicated in oxidative stress (i.e., superoxide dismutase, peroxiredoxin 6, and glutathione peroxidase). Elevated Aggregata levels in the octopuses corresponded to an increase in the expression of the cholecystokininA receptor and the small cardioactive peptide-related peptide. In contrast, we observed decreased relative expression of cephalotocin, dopamine β-hydroxylase, peptide PRQFV-amide, and tachykinin-related peptide genes. A discussion is provided on (i) potential roles of the various molecules in food intake regulation and digestive tract motility control and (ii) the difference in relative gene expression in the gastric ganglion in octopus with relatively high and low parasitic loads and the similarities to changes in the enteric innervation of mammals with digestive tract parasites. Our results provide additional data to the described neurochemical complexity of O. vulgaris gastric ganglion.

Can Cephalopods Vomit? Hypothesis Based on a Review of Circumstantial Evidence and Preliminary Experimental Observations

“…In O. vulgaris, the gastric ganglion has been shown to be involved in the control of the crop and stomach movements (Andrews and Tansey, 1983). The diversity of putative peptide and non-peptide transmitters and receptors in the gastric ganglion, its relatively large size, and complex internal organization support the proposal that it has an important function in coordinating the functions of the various regions of the digestive tract (Andrews and Tansey, 1983;Baldascino et al, 2017). It is proposed that the motility of the stomach, crop, and esophagus required for ejection of material will be coordinated by the gastric and inferior buccal ganglia, in the same way that the stomatogastric system coordinates comparable events in Pleurobranchea and Aplysia (see above).…”

“…As domoic acid is widely distributed in visceral tissues (e.g., digestive gland, posterior salivary glands, kidney, gills, and systemic heart; Costa et al, 2005) and the brain (Lopes et al, 2018), it is highly likely that the neurones in the wall of the gut and the gastric and buccal ganglia will also be exposed. The gastric ganglion has a variety of putative neurotransmitters and receptors (Andrews and Tansey, 1983;Baldascino et al, 2017), so even if glutamate receptors are present and the associated neurones are damaged, a total loss of functionality is unlikely but the ability of the gastric ganglion to coordinate digestive tract motility may be disrupted.…”

“…The gastric ganglion is implicated in the control of digestive tract motility post-prandially in cephalopods but how this occurs has not been investigated (Andrews and Tansey, 1983;Baldascino et al, 2017). By analogy with the stomatogastric nervous system in crustacea and opisthobranch mollusks (see above), control involves microcircuits, but changes in activity of such microcircuits can lead to a switch from ingestive to egestive behavior (Jing et al, 2007;Daur et al, 2016).…”

“…The contractions of the stomach combined with transient inactivity in the crop are clearly capable of pushing semi-digested food into the crop, which would be a preparatory phase for ejection via the esophagus. Note : this study used tissue removed post mortem from animals killed according to current guidelines ( Fiorito et al, 2015 ) and is not covered by EU/2010/63 ( Baldascino et al, 2017 ). The digestive tract was placed in sea water at ambient temperature (~22°C) and gassed with air; tissue remained active for at least 1 h.…”

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

“…They play a role in regulation of vasodilation and muscle contraction. In octopods, the existence of a tachykinin receptor throughout peripheral tissues and the heart suggests that these ancient roles are preserved, but in some species tachykinins have also been recruited as key active components of venom . It thus seems likely that the venom tachykinins have arisen through neofunctionalization of existing endogenous tachykinins.…”