Effect of Air Exposure-Induced Hypoxia on Neurotransmitters and Neurotransmission Enzymes in Ganglia of the Scallop Azumapecten farreri

Abstract

The nervous system expresses neuromolecules that play a crucial role in regulating physiological processes. Neuromolecule synthesis can be regulated by oxygen-dependent enzymes. Bivalves are a convenient model for studying air exposure-induced hypoxia. Here, we studied the effects of hypoxia on the expression and dynamics of neurotransmitters, and on neurotransmitter enzyme distribution, in the central nervous system (CNS) of the scallop Azumapecten farreri. We analyzed the expression of the neurotransmitters FMRFamide and serotonin (5-HT) and the choline acetyltransferase (CHAT) and universal NO-synthase (uNOS) enzymes during air exposure-induced hypoxia. We found that, in early-stage hypoxia, total serotonin content decreased in some CNS regions but increased in others. CHAT-lir cell numbers increased in all ganglia after hypoxia; CHAT probably appears de novo in accessory ganglia. Short-term hypoxia caused increased uNOS-lir cell numbers, while long-term exposure led to a reduction in their number. Thus, hypoxia weakly influences the number of FMRFamide-lir neurons in the visceral ganglion and does not affect peptide expression in the pedal ganglion. Ultimately, we found that the localization and level of synthesis of neuromolecules, and the numbers of cells expressing these molecules, vary in the scallop CNS during hypoxia exposure. This indicates their possible involvement in hypoxia resistance mechanisms.

Neurogenesis of the scallop Azumapecten farreri: from the first larval sensory neurons to the definitive nervous system of juveniles

“…The nervous system of bivalves has a ganglionic (three ganglia: CPG, PG, and VG), tetraneural (paired lateral and visceral cord) structure [ 15 , 17 , 20 , 25 , 26 ]. In scallops, the structure of the nervous system differs from other bivalves, and this is reflected in the appearance of additional neurostructures, such as additional ganglia (Ag) and nerves associated with the innervation of the unique sensory structures of the scallop such as eyes, osphradium (osphradial nerves, branchial, pallial nerves) [ 8 , 18 , 27 , 28 ].…”

“…Among the great taxonomic and ecological diversity of bivalves, scallops, which are morphologically unique bivalve mollusks, possess developed visual systems [1], muscle systems that exhibit muscle conditions (catch state [2][3][4]), an immune system [5,6], and a neurohumoral system providing complex physiological and behavioral responses of bivalves [7,8]. Among all other organ systems of mollusks, the nervous system and its neurotransmitters are of great importance in the regulation of homeostasis in general, and particularly in various physiological processes; such as regulation of locomotor activity [9], contraction of striated and smooth (catch) muscles including the heart [2,4], regulation of metabolism [10], circulation, feeding, digestion, reproduction, and osmoregulation [11][12][13][14][15].…”

Role of the Neuroendocrine System of Marine Bivalves in Their Response to Hypoxia

“…In the bivalve CNS, the organization of the 5-HT systems and 5-HT content differs between species and sexes, and is subject to seasonal variations [ 96 , 101 , 102 , 103 ]. Hypoxia exposure causes the 5-HT-immunoreactivity level to decrease in the ganglia and increase in the gills and other non-nervous tissues [ 72 , 104 ] ( Figure 3 ). These data agree with the long-established fact that 5-HT has a cilio-excitatory and metabolic stimulatory effect on the gills of several bivalve mollusks [ 62 , 72 , 74 , 75 , 105 , 106 ] ( Figure 2 ).…”

“…In bivalves exposed to chronic hypoxia, the 5-HT level in the CNS has been found to decrease [ 104 ] ( Figure 3 ), while the level of 5-HT in the hemolymph and mantle may increase significantly against air exposure stress [ 56 ]. In Pacific oysters ( Crassostrea gigas ) after exposure to air for 24 h, the high concentration of 5-HT in the hemolymph may decrease the apoptosis rate of hemocytes.…”

“…Biochemical and histochemical studies on mollusks have demonstrated the presence of the enzyme synthesizing acetylcholine (CHAT) and the enzyme hydrolyzing it (acetylcholinesterase, AChE) in a multitude of taxonomic groups [ 36 , 104 , 132 , 135 , 136 , 137 ]. Furthermore, substantial homologies have been found between the ACh receptors cloned to date from invertebrate and vertebrate animals [ 138 , 139 ].…”