Evidence for a widespread involvement of NO in control of photogenesis in bioluminescent fish

Abstract

Krönström, J. and Mallefet, J. 2010. Evidence for a widespread involvement of NO in control of photogenesis in bioluminescent fish. -Acta Zoologica (Stockholm) 91: 474-483.The presence of nitric oxide synthase (NOS) and nerve fibres in the photophores of seven bioluminescent fish species (Hygophum benoiti, Myctophum punctatum, Electrona risso, Cyclothone braueri, Vinciguerria attenuata, Maurolicus muelleri and Porichthys notatus) with endogenous photocytes, were investigated. Antibodies directed against neuronal and inducible NOS (n and iNOS respectively) and NADPH-diaphorase activity were used to reveal the locations of NOS, while antibodies directed against acetylated tubulin were used to visualize nerve fibres. The nNOS antibody labelled structures in all investigated photophores except in the organs from P. notatus. The photocytes of P. notatus showed NADPH-diaphorase activity. In the myctophid species, NOS-like immunoreactivity was found in small intracellular structures of the photocytes and in nerve fibres reaching the photocytes. nNOS-positive fibres were also found among lens ⁄ filter cells in V. attenuata, and in M. muelleri the cytoplasm of lens ⁄ filter cells contained NOSlike material. In C. braueri, a cell type located at a collecting chamber for luminous products in the photophore contained NOS-like material. All photophores received an innervation reaching the photocytes, as well as other components including lens ⁄ filter areas. The results of this study comply with an involvement of nitric oxide in the control of bioluminescence in several fish species.

Nitric oxide in the control of luminescence from lantern shark (Etmopterus spinax) photophores

“…The presence of NOS in the caudal organ of the myctophid M. punctatum (Krönström and Mallefet, 2009), which is probably used for sexual communication (Herring, 2007), supports the idea that the effects of NO on luminescence are not restricted to the counterilluminating behaviour in fishes. It is therefore possible that NO modulation also exists in luminous zones of E. spinax that are not involved in counterillumination, but this needs further analysis.…”

“…In the hatchetfish (A. hemigymnus), the NO modulation of adrenaline-induced luminescence appears to occur via nerves reaching the photocytes, and other luminescent bony fish harbour NOcontaining nerves inside their photogenic organs (Krönström et al, 2005;Krönström and Mallefet, 2009). No clear evidence of such NOcontaining nerves was found in the photophores of the cartilaginous E. spinax.…”

“…In a recent study, it was suggested that NO could be involved in the control of light production/emission of many luminescent teleost fish species (Krönström and Mallefet, 2009). Our results confirm this idea and show that cartilaginous luminescent fish also evolved a NO regulation system for their luminescence.…”

“…Its effects are mediated either by the production of cyclic guanosine monophosphate (cGMP) or by the inhibition of mitochondrial respiration in the target cells (Brown, 1995;Jacklet, 1997). Since several recent studies demonstrated the involvement of NO as a neuromodulator of neurally induced luminescence from distantly related marine organisms, such as the northern krill Meganyctiphanes norvegica (Krönström et al, 2007) and teleost fish species including the hatchetfish Argyropelecus hemigymnus (Krönström et al, 2005) and the midshipman fish Porichthys notatus (Krönström, 2009;Krönström and Mallefet, 2009), we investigated the possible role of NO in the modulation of hormonally induced luminescence in the cartilaginous fish E. spinax.…”

The first report of luminescent liver tissue in fishes: Evolution and structure of bioluminescent organs in the deep-sea naked barracudinas (Aulopiformes: Lestidiidae)

“…D and C). Other dermal light organs in the distantly related stomiiform, myctophiform, and batrachoidiform fishes also have photogenic cells with granular inclusions that likely fuse with vacuoles or release their content into ducts or an extracellular space as a component of light production (Nicol, ; Copeland, ; Herring and Cope, ; Krönström and Mallefet, ; Cavallaro et al, ). The sinuses found in both luminescent organs are suggestive that the light –production mechanism in both organs may involve extracellular secretion.…”