Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, <i>Meganyctiphanes norvegica</i> (M. Sars)

SUMMARYThe barnacle Balanus amphitrite is among the most dominant fouling species on intertidal rocky shores in tropical and subtropical areas and is thus a target organism in antifouling research. After being released from adults, the swimming nauplius undertakes six molting cycles and then transforms into a cyprid. Using paired antennules, a competent cyprid actively explores and selects a suitable substratum for attachment and metamorphosis (collectively known as settlement). This selection process involves the reception of exogenous signals and subsequent endogenous signal transduction. To investigate the involvement of nitric oxide (NO) and cyclic GMP (cGMP) during larval settlement of B. amphitrite, we examined the effects of an NO donor and an NO scavenger, two nitric oxide synthase (NOS) inhibitors and a soluble guanylyl cyclase (sGC) inhibitor on settling cyprids. We found that the NO donor sodium nitroprusside (SNP) inhibited larval settlement in a dose-dependent manner. In contrast, both the NO scavenger carboxy-PTIO and the NOS inhibitors aminoguanidine hemisulfate (AGH) and S-methylisothiourea sulfate (SMIS) significantly accelerated larval settlement. Suppression of the downstream guanylyl cyclase (GC) activity using a GC-selective inhibitor ODQ could also significantly accelerate larval settlement. Interestingly, the settlement inhibition effects of SNP could be attenuated by ODQ at all concentrations tested. In the developmental expression profiling of NOS and sGC, the lowest expression of both genes was detected in the cyprid stage, a crucial stage for the larval decision to attach and metamorphose. In summary, we concluded that NO regulates larval settlement via mediating downstream cGMP signaling. Supplementary material available online at

Section: Discussionmentioning

confidence: 99%

The regulatory role of the NO/cGMP signal transduction cascade during larval attachment and metamorphosis of the barnacleBalanus (=Amphibalanus) amphitrite

Zhang

et al. 2012

“…Indeed, although NO is known to J. M. Claes, H.-C. Ho and J. Mallefet modulate the hormonally induced luminescence in E. spinax (Claes et al, 2010c), it did not have any effect on MT-induced luminescence from S. aliae photophores. Effects of NO on the luminescence of marine organisms are, however, known to be versatile and complex (Krönström et al, 2005;Krönström et al, 2007;Claes et al, 2010c), and additional experiments are certainly needed to completely exclude NO from the pygmy shark luminescence control.…”

Section: Control Of Pygmy Shark Luminescencementioning

confidence: 99%

Control of luminescence from pygmy shark (Squaliolus aliae) photophores

Claes

Mallefet

2012

SUMMARYThe smalleye pygmy shark (Squaliolus aliae) is a dwarf pelagic shark from the Dalatiidae family that harbours thousands of tiny photophores. In this work, we studied the organisation and physiological control of these photogenic organs. Results show that they are mainly situated on the ventral side of the shark, forming a homogeneous ventral photogenic area that appears well suited for counterillumination, a well-known camouflage technique of pelagic organisms. Isolated ventral skin patches containing photophores did not respond to classical neurotransmitters and nitric oxide but produced light after melatonin (MT) application. Prolactin and a-melanocyte-stimulating hormone inhibited this hormonally induced luminescence as well as the spontaneous luminescence from the photogenic tissue. The action of MT seems to be mediated by binding to the MT 2 receptor subtype, as the MT 2 receptor agonist 4P-PDOT inhibited the luminescence induced by this hormone. Binding to this receptor probably decreases the intracellular cAMP concentration because forskolin inhibited spontaneous and MT-induced luminescence. In addition, a GABA inhibitory tonus seems to be present in the photogenic tissue as well, as GABA inhibited MT-induced luminescence and the application of bicuculline provoked luminescence from S. aliae photophores. Similarly to what has been found in Etmopteridae, the other luminous shark family, the main target of the luminescence control appears to be the melanophores covering the photocytes. Results suggest that bioluminescence first appeared in Dalatiidae when they adopted a pelagic style at the Cretaceous/Tertiary boundary, and was modified by Etmopteridae when they started to colonize deep-water niches and rely on this light for intraspecific behaviours.

“…In northern krill, serotonin is the primary regulatory biogenic amine (Fregin and Wiese, 2002;Kronstrom et al, 2007). Serotonergic neurons innervate muscular sphincters that regulate the access of haemolymph to the light organ, thus serotonin regulates the flow of oxygenated haemolymph to the light organ, modulating the bioluminescence reaction (Kronstrom et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Serotonergic neurons innervate muscular sphincters that regulate the access of haemolymph to the light organ, thus serotonin regulates the flow of oxygenated haemolymph to the light organ, modulating the bioluminescence reaction (Kronstrom et al, 2007). In fireflies, regulation of oxygen supply to the light organ also seems to be the key regulator of bioluminescence.…”

Section: Introductionmentioning

confidence: 99%

Roles of biogenic amines in regulating bioluminescence in the Australian glowworm Arachnocampa flava

Rigby

Merritt

2011

SUMMARY The glowworm Arachnocampa flava is a carnivorous fly larva (Diptera) that uses light to attract prey into its web. The light organ is derived from cells of the Malpighian tubules, representing a bioluminescence system that is unique to the genus. Bioluminescence is modulated through the night although light levels change quite slowly compared with the flashing of the better-known fireflies (Coleoptera). The existing model for the neural regulation of bioluminescence in Arachnocampa, based on use of anaesthetics and ligations, is that bioluminescence is actively repressed during the non-glowing phase and the repression is partially released during the bioluminescence phase. The effect of the anaesthetic, carbon dioxide, on the isolated light organ from the present study indicates that the repression is at least partially mediated at the light organ itself rather than less directly through the central nervous system. Blocking of neural signals from the central nervous system through ligation leads to uncontrolled release of bioluminescence but light is emitted at relatively low levels compared with under anaesthesia. Candidate biogenic amines were introduced by several methods: feeding prey items injected with test solution, injecting the whole larva, injecting a ligated section containing the light organ or bathing the isolated light organ in test solution. Using these methods, dopamine, serotonin and tyramine do not affect bioluminescence output. Exposure to elevated levels of octopamine via feeding, injection or bathing of the isolated light organ indicates that it is involved in the regulation of repression. Administration of the octopamine antagonists phentolamine or mianserin results in very high bioluminescence output levels, similar to the effect of anaesthetics, but only mianserin acts directly on the light organ.