Control of Bioluminescence in Myctophid Fishes

Indian Journal of Geo Marine Science Vol. 46 (07), July 2017, pp. 1436-1439

Control of bioluminescence in Myctophid ﬁshes

Abhay Deshmukh

Centre for Marine Living Resources & Ecology (CMLRE) Kochi, Pin-682037, India

Received 17 September 2014 ; revised 16 October 2014

Bioluminescence crosses all oceanic dimensions and has evolved many times from bacteria to fish to powerfully influence behavioral and ecosystem dynamics. Luminous fishes make up a major portion of the oceans' mid- and deep-water fauna. However, in only a few of these the mechanism of luminescence well understood. Myctophids, or lanternfishes, are among the most abundant group of mesopelagic fishes in the World's oceans. They range from the Arctic to the Antarctic and, as a result of their diurnal migrations, can be found from the surface waters down to depths exceeding 2000 m. They have small photophores pointed downward and to the side, as well as large photophores on the tail, which can produce bright, fast flashes. In spite of the vast quantity of research directed towards myctophids, there are still few or no firm results regarding control of bioluminescence in myctophids.

[Keywords: Bioluminescence, Myctophid, photophores, mesopelagic, fish]

Introduction The vast majority of bioluminescent organisms Bioluminescence spans all oceanic dimensions reside in the ocean; of the more than 700 genera and has evolved many times from bacteria to fish known to contain luminous species, some 80% are to powerfully influence behavioral and ecosystem marine. These occupy a diverse range of habitats, dynamics. Luminescence is very common among from polar to tropical and from surface waters to marine animals, and many species possess highly the sea floor1.’’ A survey around Bermuda developed photophores or light-emitting organs. It indicated that 97% of fishes living between 500 is probable; therefore, that luminescence plays an and 1000m are bioluminescent2. Bioluminescence important part in the economy of their lives. The reflect the unique nature of the visual relative importance of bioluminescence varies environment in which they have evolved. Open over the course of a day; at night it is the only ocean is a world without hiding places, where light source available for vision within the sunlight filtering down through clear water mesopelagic environment. diminishes approximately 10-fold for every 75 m Myctophids are major components of the of decent, until all visible light disappears below mesopelagic fauna throughout the world ocean. 1000 m. Under sunlight or moonlight, the light Myctophids, or lanternfishes, are extremely field is dim, blue, and highly directional. In order abundant in the midwater, migrating near the to hide, many animals vertically migrate surface at night. Bioluminesence in myctophids is downward into the dark depths during the day and still a mystery even after a great extent work is only venture into food rich surface waters under done on myctophids. The general inability to cover of darkness. With increasing depth not only identify a mode of luminescence in myctophids does the intensity of sunlight fall in an (as well as some other luminous fishes) has led to approximately exponential manner, but the a default assumption that the fishes are spectral quality of this light also changes, themselves responsible for their luminescence, becoming increasingly restricted to a narrow with the genes encoding luciferase residing on the waveband of light (470–490 nm)3. The decrease fish chromosome4,5.’’ From this, Two hypotheses in sunlight with depth is met with an increase in Can be proposed 1) that these fishes have evolved the relative importance of bioluminescent point their own method of luminescence (presumably sources produced by marine fauna. independently) or 2) that these fishes have

INDIAN J. MAR. SCI., VOL. 46, NO. 07, JULY 2017 1437 incorporated the genes necessary for and its significance could not be assessed9. luminescence via lateral gene transfer from According to him Forans positive result for luminous bacteria, circumventing the need for a bacterial symbionts could be because of 1. The symbiont. In this review article we have tried to presence of bacterial symbionts, 2. Contamination discuss various possibilities which grounds of specimens with luminescence bacteria, possibly bioluminescence in myctophid. from the intestinal content expelled by organism in the trawl, or free leaving sea water bacteria, or Is bioluminescence in myctophid fishes due to 3. Contamination with DNA containing luciferase bacterial luciferase? genes during processing in the laboratory. Haygood conducted the similar experiment again Bacterial luciferase is a heterodimeric enzyme of but used dissected photophores as a source of 77 kDa, composed of α and β subunits with DNA rather than muscle and skin. Hibridization molecular masses of 40 and 37 kDa, respectively. with lux probes did not detect lux sequences in The two polypeptides are encoded on closely photophore DNA from three species of linked adjacent genes, luxA and luxB6.’’ myctophids, they concluded that there is no The mechanism of the bioluminescence reaction evidence of bacterial luciferace in the in bacteria is catalyzed by luciferase, this reaction bioluminescence in myctophids9. have been studied extensively, primarily because of the very slow turnover of the enzyme. The Bioluminescence in Myctophid is attributed to a reduced flavin, FMNH2, bound to the enzyme, coelenterazine based system reacts with 02 to form a 4a-peroxyflavin. This complex interacts with aldehyde to form a highly Bioluminescence is light produced by a chemical stable intermediate, which decays slowly, reaction within a living organism. At least two resulting in the emission of light along with the chemicals plus oxygen are required. The chemical oxidation of the substrates. Bacterial luciferase that produces the light is generically called activity was detected in light organ extracts of luciferin, and the chemical that drives or catalyzes squids, fishes, and pyrosomes, suggesting that the reaction is called lucerifase. The chemical these systems are derived from bacteria-animal reaction is very efficient, producing 98% of its symbioses7, this finding make us to think over the energy as light (glow) and only 2% as heat. One possibility of similar mechanism in myctophid. photon of light is produced for each molecule of Bioluminescence of myctophids and some luciferin consumed. Specific luciferin Biolume stomiiform fishes is due to bacterial symbionts in used is called coelenterazine, a word derived from their photophores, based on positive hybridization coelenterates, a class of marine invertebrates that of bacterial luminescence (lux) gene probes to includes jellyfish, sea anemones, and corals. DNA from muscle and skin of myctophids and in Coelenterazine is the most widespread luciferin situ hybridization8. In this study, labeled molecule found in nature. It is a very potent, luciferase gene fragments from luminous marine natural anti-oxidant. All of the marine organisms bacteria were used to probe DNA isolated from that emit light use different luciferases but most specific fish tissues. A positive signal was use the same luciferin, coelenterazine. obtained from skin DNA in all luminous fishes Photophore extracts of the myctophid, Diaphus examined, whereas muscle DNA gave a weaker elucens Brauer, cross-react to give light with signal and brain DNA was negative. This highly purified luciferin (substrate) and luciferase observation is consistent with luminous bacteria (enzyme) of the marine ostracod crustacean, acting as the light source in myctophids and Cypridina hilgendorfii. From this study they argues against the genes necessary for concluded that the myctophid species reported luminescence residing on the fish chromosomes. here have the biochemical mechanism for Haygood opposed Forans studies which says that luminescence involving luceferin and luciferase10. bacterial symbiots are responsible for All organisms do not synthesize the luceferin luminescence in myctophids, according to him molecule. In some cases luciferin is acquired although bacterial luminescence (lux) gene probes exogenously through the diet11,12,13 14..Because derived from luminescence bacterium Vibrio luciferins are present in both luminous and non fischeri were hybridized to DNA from mussel, luminous marine animals15,16, they are relatively skin and brain, but no positive controls, such as easy to obtain. But because the complete luminous bacterial cultures or sample from animal biosynthesis pathway is not yet known for any known to be symbiotically luminous, were marine luciferins, their ultimate origins remain included, thus the relative strength of the signal unknown.

1438 DESHMUKH: CONTROL OF BIOLUMINESCENCE IN MYCTOPHID FISHES

Bioluminescence due to light switch in Several recent studies have demonstrated the photophores involvement of NO as a neuromodulator of neutrally induced luminescence from distantly As observers, we typically encounter related marine organisms, such as the northern bioluminescence in organisms that have been krill29 Meganyctiphanes norvegica and teleost fish induced to flash by a physical disturbance. In a species including the hatchet fish30 Argyropelecus natural context, however, the emission of light is hemigymnus and the midshipman fish31,32 closely controlled by chemical and neurological Porichthys notatus. Kronstrom and Mallefet’s mechanisms. Animals can turn their photophores studies reached to conclusion that, NOS (nitric on and off, but they can also modulate the oxide synthase) like immunoreactivity was found intensity, colour, and even angular distribution of in small intracellular structures of the photocytes light. These control mechanisms often involve and in nerve fibres reaching the photocytes of calcium ions and other standard neurotransmitters. myctophid. Intracellular location of NOS-like Myctophid species (Electrona risso, Hygophum material in small dot- or stripe-like structures was benoiti and Myctophum punctatum, observed in the ventral photocytes. Dot like Myctoformes:Myctophidae) all have similar, but structures were distributed in the whole cytoplasm not identical, cup-shaped ventral photophores as well as close to the cell membranes30. This with a small group of long flattened photocytes study suggested that NO is involved in either the (light-producing cells). The scales over the control of light production or in the modulation of photocytes are modified and act like a lens. light. Caudal organs contain more abundant flattened photocytes, connected as a syncytium17,18,19. Conclusion Studies of the control of the myctophid While the genes for many luciferases are known, photophores are either lacking or have often failed the mechanisms of luciferin biosynthesis are due to the difficulties with capturing and almost entirely unknown. Working on this aspect maintaining live animals21,22,23. No endogenous will be a promising area for future research. A substances tested so far adrenaline20, better access to live animals in good condition noradrenaline, acetylcholine21, induce a will give opportunities to understand natural reproducible luminescence response in myctophid functions of luminescence. The question of why species, but both ventral and caudal photophores Myctophids are bioluminescent still does not have from M. Punctatum respond to electrical a satisfactory answer. Although there have been stimulation. Microscopy studies indicate that both breakthroughs in understanding the molecular types of myctophid photophores (ventral and basis for the major luminescence systems, the caudal) are under nervous control17,18,22. chemistry of luminescence for myctophid still In contrast, intact specimens of M. muelleri and remains a disguise. isolated photophores from P. notatus consistently respond to injection of adrenaline and application Acknowledgement of adrenaline or noradrenaline, respectively20,23. Authors are thankful to the Director, CMLRE for C. braueri photophores respond to submersion of his constant help and encouragement. The an intact fish in adrenaline (J Mallefet, financial and logistical support from the Centre unpublished data). Adrenaline stimulates light for Marine Living Resources and Ecology production from the photocytes when applied to (CMLRE), Ministry of Earth Sciences (MoES), is isolated photophores24,25. Mallefet and Baguet25 thankfully acknowledged. By taking in to consideration the active role of adrenaline in luminescence25, involvement of References nitric oxide (NO) which is considered to be 1. Widder, E.A. (2010) Bioluminescence in the modulator of the adrenaline induced light ocean: origins of biological, chemical, and production was studied On myctophid species26. ecological diversity. Sci. 328, 704-708. 2. Beebe, W. M. (1937): Preliminary list of Bermuda Nitric oxide (NO) is a small gaseous signalling deep-sea fishes. Zoologica, N.Y. 22, 197–208. molecule that plays a key role in invertebrate as 3. Turner, J.R., White, E.M., Collins, M.A., Partridge, well as in vertebrate biological functions27.Its J.C. and Douglas, R.H. (2009): Vision in effects are mediated either by the production of lanternfish (Myctophidae): adaptations for viewing bioluminescence in the deep-sea. Deep Sea Res. I cyclic guanosine monophosphate (cGMP) or by 56:1003–17 the inhibition of mitochondrial respiration in the target cells27,28.

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