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

[E-mail: adeshmukh0110@gmail.com]

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

reside in the ocean; of the more than 700 genera

known to contain luminous species, some 80% are

marine. These occupy a diverse range of habitats,

from polar to tropical and from surface waters to

the sea floor1.’’ A survey around Bermuda

indicated that 97% of fishes living between 500

and 1000m are bioluminescent2. Bioluminescence

reflect the unique nature of the visual

environment in which they have evolved. Open

ocean is a world without hiding places, where

sunlight filtering down through clear water

diminishes approximately 10-fold for every 75 m

of decent, until all visible light disappears below

1000 m. Under sunlight or moonlight, the light

field is dim, blue, and highly directional. In order

to hide, many animals vertically migrate

downward into the dark depths during the day and

only venture into food rich surface waters under

cover of darkness. With increasing depth not only

does the intensity of sunlight fall in an

approximately exponential manner, but the

spectral quality of this light also changes,

becoming increasingly restricted to a narrow

waveband of light (470–490 nm)3. The decrease

in sunlight with depth is met with an increase in

the relative importance of bioluminescent point

sources produced by marine fauna.

Bioluminescence spans all oceanic dimensions

and has evolved many times from bacteria to fish

to powerfully influence behavioral and ecosystem

dynamics. Luminescence is very common among

marine animals, and many species possess highly

developed photophores or light-emitting organs. It

is probable; therefore, that luminescence plays an

important part in the economy of their lives. The

relative importance of bioluminescence varies

over the course of a day; at night it is the only

light source available for vision within the

mesopelagic environment.

Myctophids are major components of the

mesopelagic fauna throughout the world ocean.

Myctophids, or lanternfishes, are extremely

abundant in the midwater, migrating near the

surface at night. Bioluminesence in myctophids is

still a mystery even after a great extent work is

done on myctophids. The general inability to

identify a mode of luminescence in myctophids

(as well as some other luminous fishes) has led to

a default assumption that the fishes are

themselves responsible for their luminescence,

with the genes encoding luciferase residing on the

fish chromosome4,5

.’’ From this, Two hypotheses

Can be proposed 1) that these fishes have evolved

their own method of luminescence (presumably

independently) or 2) that these fishes have

INDIAN J. MAR. SCI., VOL. 46, NO. 07, JULY 2017

incorporated the genes necessary for

luminescence via lateral gene transfer from

luminous bacteria, circumventing the need for a

symbiont. In this review article we have tried to

discuss various possibilities which grounds

bioluminescence in myctophid.

Is bioluminescence in myctophid fishes due to

bacterial luciferase?

Bacterial luciferase is a heterodimeric enzyme of

77 kDa, composed of α and β subunits with

molecular masses of 40 and 37 kDa, respectively.

The two polypeptides are encoded on closely

linked adjacent genes, luxA and luxB6.’’

The mechanism of the bioluminescence reaction

in bacteria is catalyzed by luciferase, this reaction

have been studied extensively, primarily because

of the very slow turnover of the enzyme. The

reduced flavin, FMNH2, bound to the enzyme,

reacts with 02 to form a 4a-peroxyflavin. This

complex interacts with aldehyde to form a highly

stable intermediate, which decays slowly,

resulting in the emission of light along with the

oxidation of the substrates. Bacterial luciferase

activity was detected in light organ extracts of

squids, fishes, and pyrosomes, suggesting that

these systems are derived from bacteria-animal

symbioses7, this finding make us to think over the

possibility of similar mechanism in myctophid.

Bioluminescence of myctophids and some

stomiiform fishes is due to bacterial symbionts in

their photophores, based on positive hybridization

of bacterial luminescence (lux) gene probes to

DNA from muscle and skin of myctophids and in

situ hybridization8. In this study, labeled

luciferase gene fragments from luminous marine

bacteria were used to probe DNA isolated from

specific fish tissues. A positive signal was

obtained from skin DNA in all luminous fishes

examined, whereas muscle DNA gave a weaker

signal and brain DNA was negative. This

observation is consistent with luminous bacteria

acting as the light source in myctophids and

argues against the genes necessary for

luminescence residing on the fish chromosomes.

Haygood opposed Forans studies which says that

bacterial symbiots are responsible for

luminescence in myctophids, according to him

although bacterial luminescence (lux) gene probes

derived from luminescence bacterium Vibrio

fischeri were hybridized to DNA from mussel,

skin and brain, but no positive controls, such as

luminous bacterial cultures or sample from animal

known to be symbiotically luminous, were

included, thus the relative strength of the signal

and its significance could not be assessed9.

According to him Forans positive result for

bacterial symbionts could be because of 1. The

presence of bacterial symbionts, 2. Contamination

of specimens with luminescence bacteria, possibly

from the intestinal content expelled by organism

in the trawl, or free leaving sea water bacteria, or

3. Contamination with DNA containing luciferase

genes during processing in the laboratory.

Haygood conducted the similar experiment again

but used dissected photophores as a source of

DNA rather than muscle and skin. Hibridization

with lux probes did not detect lux sequences in

photophore DNA from three species of

myctophids, they concluded that there is no

evidence of bacterial luciferace in the

bioluminescence in myctophids9.

Bioluminescence in Myctophid is attributed to a

coelenterazine based system

Bioluminescence is light produced by a chemical

reaction within a living organism. At least two

chemicals plus oxygen are required. The chemical

that produces the light is generically called

luciferin, and the chemical that drives or catalyzes

the reaction is called lucerifase. The chemical

reaction is very efficient, producing 98% of its

energy as light (glow) and only 2% as heat. One

photon of light is produced for each molecule of

luciferin consumed. Specific luciferin Biolume

used is called coelenterazine, a word derived from

coelenterates, a class of marine invertebrates that

includes jellyfish, sea anemones, and corals.

Coelenterazine is the most widespread luciferin

molecule found in nature. It is a very potent,

natural anti-oxidant. All of the marine organisms

that emit light use different luciferases but most

use the same luciferin, coelenterazine.

Photophore extracts of the myctophid, Diaphus

elucens Brauer, cross-react to give light with

highly purified luciferin (substrate) and luciferase

(enzyme) of the marine ostracod crustacean,

Cypridina hilgendorfii. From this study they

concluded that the myctophid species reported

here have the biochemical mechanism for

luminescence involving luceferin and luciferase10

.

All organisms do not synthesize the luceferin

molecule. In some cases luciferin is acquired

exogenously through the diet11,12,13 14

..Because

luciferins are present in both luminous and non

luminous marine animals15,16

, they are relatively

easy to obtain. But because the complete

biosynthesis pathway is not yet known for any

marine luciferins, their ultimate origins remain

unknown.

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DESHMUKH: CONTROL OF BIOLUMINESCENCE IN MYCTOPHID FISHES

Bioluminescence due to light switch in

photophores

As observers, we typically encounter

bioluminescence in organisms that have been

induced to flash by a physical disturbance. In a

natural context, however, the emission of light is

closely controlled by chemical and neurological

mechanisms. Animals can turn their photophores

on and off, but they can also modulate the

intensity, colour, and even angular distribution of

light. These control mechanisms often involve

calcium ions and other standard neurotransmitters.

Myctophid species (Electrona risso, Hygophum

benoiti and Myctophum punctatum,

Myctoformes:Myctophidae) all have similar, but

not identical, cup-shaped ventral photophores

with a small group of long flattened photocytes

(light-producing cells). The scales over the

photocytes are modified and act like a lens.

Caudal organs contain more abundant flattened

photocytes, connected as a syncytium17,18,19

.

Studies of the control of the myctophid

photophores are either lacking or have often failed

due to the difficulties with capturing and

maintaining live animals21,22,23

. No endogenous

substances tested so far adrenaline20

,

noradrenaline, acetylcholine21

, induce a

reproducible luminescence response in myctophid

species, but both ventral and caudal photophores

from M. Punctatum respond to electrical

stimulation. Microscopy studies indicate that both

types of myctophid photophores (ventral and

caudal) are under nervous control17,18,22

.

In contrast, intact specimens of M. muelleri and

isolated photophores from P. notatus consistently

respond to injection of adrenaline and application

of adrenaline or noradrenaline, respectively20,23

.

C. braueri photophores respond to submersion of

an intact fish in adrenaline (J Mallefet,

unpublished data). Adrenaline stimulates light

production from the photocytes when applied to

isolated photophores24

,25

. Mallefet and Baguet25

By taking in to consideration the active role of

adrenaline in luminescence25, involvement of

nitric oxide (NO) which is considered to be

modulator of the adrenaline induced light

production was studied On myctophid species26

.

Nitric oxide (NO) is a small gaseous signalling

molecule that plays a key role in invertebrate as

well as in vertebrate biological functions27

.Its

effects are mediated either by the production of

cyclic guanosine monophosphate (cGMP) or by

the inhibition of mitochondrial respiration in the

target cells27,28

.

Several recent studies have demonstrated the

involvement of NO as a neuromodulator of

neutrally induced luminescence from distantly

related marine organisms, such as the northern

krill29

Meganyctiphanes norvegica and teleost fish

species including the hatchet fish30

Argyropelecus

hemigymnus and the midshipman fish31,32

Porichthys notatus. Kronstrom and Mallefet’s

studies reached to conclusion that, NOS (nitric

oxide synthase) like immunoreactivity was found

in small intracellular structures of the photocytes

and in nerve fibres reaching the photocytes of

myctophid. Intracellular location of NOS-like

material in small dot- or stripe-like structures was

observed in the ventral photocytes. Dot like

structures were distributed in the whole cytoplasm

as well as close to the cell membranes30

. This

study suggested that NO is involved in either the

control of light production or in the modulation of

light.

Conclusion

While the genes for many luciferases are known,

the mechanisms of luciferin biosynthesis are

almost entirely unknown. Working on this aspect

will be a promising area for future research. A

better access to live animals in good condition

will give opportunities to understand natural

functions of luminescence. The question of why

Myctophids are bioluminescent still does not have

a satisfactory answer. Although there have been

breakthroughs in understanding the molecular

basis for the major luminescence systems, the

chemistry of luminescence for myctophid still

remains a disguise.

Acknowledgement Authors are thankful to the Director, CMLRE for

his constant help and encouragement. The

financial and logistical support from the Centre

for Marine Living Resources and Ecology

(CMLRE), Ministry of Earth Sciences (MoES), is

thankfully acknowledged.

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