Photocyte

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A photocyte is a cell that specializes in catalyzing enzymes to produce light (bioluminescence). [1] Photocytes typically occur in select layers of epithelial tissue, functioning singly or in a group, or as part of a larger apparatus (a photophore). They contain special structures called photocyte granules. These specialized cells are found in a range of multicellular animals including ctenophora, coelenterates (cnidaria), annelids, arthropoda (including insects) and fishes. Although some fungi are bioluminescent, they do not have such specialized cells. [1]

Contents

Mechanism of light production

Light production may first be triggered by nerve impulses which stimulate the photocyte to release the enzyme luciferase into a "reaction chamber" of luciferin substrate. In some species the release occurs continually without the precursor impulse via osmotic diffusion. Molecular oxygen is then actively gated through surrounding tracheal cells which otherwise limit the natural diffusion of oxygen from blood vessels; the resulting reaction with the luciferase and luciferin produces light energy and a by-product (usually carbon dioxide). [1] The reaction occurs in the peroxisome of the cell. [2]

Researchers once postulated that ATP was the source of reaction energy for photocytes, but since ATP only produces a fraction of the energy of the luciferase reaction, any resulting light wave-energy would be too small for detection by a human eye. The wavelengths produced by most photocytes fall close to 490 nm; although light as energetic as 250 nm is reportedly possible. [1]

The variations of color seen in different photocytes are usually the result of color filters that alter the wavelength of the light prior to exiting the endoderm, thanks to the other parts of the photophore. The range of colors varies between bioluminescent species.

The exact combinations of luciferase and luciferin types found among photocytes are specific to the species to which they belong. This would seem to be the result of consistent evolutionary divergence. [1]

Anatomy and physiology

Firefly larvae

Light production in Photurius pennsylvanica larvae occurs in the roughly 2,000 photocytes located in the heavily innervated light organ of the insect which is much simpler than that of the adult organism. [3] The transparent photocytes of the larvae are clearly distinguishable from the opaque dorsal layer cells that cover them. Nervous and intracellular mechanisms contribute to light production in the photocytes. Nervous and intracellular mechanisms contribute to light production in the photocytes. It has been shown that fireflies can modify the amount of oxygen that travels through their trachea system to the light organ which plays a role in oxygen availability for light production. They do this by modifying the amount of fluid present within the trachea system. Because oxygen diffuses more slowly through water than in a gaseous form, this allows fireflies to effectively change the amount of oxygen reaching the photocytes. [4] Spiracles can be opened and closed to control the amount of air that is able to pass through the tracheal system, but this control mechanism is only used as a response to a stressor. [5]

Neural mechanism of light production

Research has shown that applying 5 to 15 volts of electricity for 50 ms to the segmental nerve that innervates the light organ leads to a glow 1.5 seconds after that lasts for five to ten seconds. Stimulation of the segmental nerve has been found to lead to several different nerve impulses, and frequency of nervous impulses has been found to be proportional to the intensity of the stimulus applied. A high frequency of nervous impulse was found to lead to a constant latency. The light organ is inactive in the absence of nerve impulses. Constant nerve signaling was shown to coincide with constant emission of light from the light organ with a higher frequency coinciding with a higher amplitude of light emitted up to 30 impulses per second. Impulses beyond this frequency were not found to be associated with a more intense glow. The fact that the frequency of nerve impulses was able to exceed beyond the maximum intensity of light emission suggests some limitations in the mechanism either arising from the synapse or the cell's light producing process. Additionally, a series of action potentials have been shown to lead to the sporadic, discontinuous emission to light. It was also found that a higher frequency of action potentials lead to a higher likelihood of any emission of light. Nerve impulses are associated with a depolarization of the photocyte which plays a role in its light emitting mechanism, and greater depolarization events were found to be associated with more intense lightning. The nerve innervating the light organ containing photocytes has only two axons, but they branch repeatedly allowing the numerous photocytes to be innervated with each cell being associated with several nerve terminals with each terminal possibly being associated with several synapses. [3]

It was found that the junction between at the end of the neuron innervating the light organ differs from the kind of junction found between two different neurons or between neurons and muscles in the neuromuscular junction. The depolarization of the photocyte following nervous stimulation was found to be one-hundred times slower than the with the other two kinds of junctions and this slow response cannot be attributed to the rate of diffusion because the synapse between the neuron and photocyte is relatively small. [3] It has been found that the neurons that control the light mechanism terminate at the tracheal cells rather than the photocytes themselves. [4]

Intracellular mechanism

The resting potential of photocytes was found to exist in a range between 50 and 65 millivolts. It is generally accepted that the emission of light was found to occur after depolarization of the photocyte membrane although some have argued that the depolarization follows the emission of light. The depolarization of the membrane results in an increase of the rate of diffusion of ions across it. The depolarization of the photocyte was found to occur 0.5 seconds following nervous impulse culminating at one second with the maximum degree of depolarization observed. A higher frequency of nervous stimulation was associated with a smaller depolarization event. Exposure to neurotransmitters including epinephrine, norepinephrine, and synephrine, results in the emission of light but without any corresponding depolarization of the photocyte membrane. [3]

Mnemiopsis leidyi

Photocytes are found distributed unevenly near the plate cilia cells. Gastric cells form a barrier that keep the photocytes away from the opening of the radially canal which they are found to exist along. [6]

Porichthys

Light production in Porichthys notatus has been found to be triggered through an adrenergic mechanism. The sympathetic nervous system of the fish is responsible for triggering bioluminescence in the photocytes. As a response to being triggered by an norepinephrine, epinephrine, or phenylephrine, the photocyte exhibits a quick flash and then emits light that slowly fades in intensity. Stimulation by isoproterenol was found to cause an only a slow fading illumination. The amplitude of the quick flash, referred to as the "fast response", was higher when the concentration of neurotransmitter stimulating it increased. A great dal of variation in luminescence was exhibited in the photocytes of different fish. Variation also existed depending on what time of year the photocytes were collected from the fish. Stimulation from phenylephrine was found to produce a less intense response than that of epinephrine or norepinephrine. Phentolamine was shown to inhibit the effect of stimulation by phenylephrine completely and of epinephrine and norepinephrine to a lesser degree. Clonidine was shown to have an inhibitory effect on the fast response but no effect on the slow response. [7] The photocytes of Porichthys are known to be extensively innervated.

Amphiura filiformis

Mechanical stimulation to spines on the arm can cause Amphiura filiformis to bioluminesce in the blue range. The species has been found to possess a luciferase compound. The luciferase has been isolated to clusters of photocytes that exist at the tip off the arms and around the spines. What are believed to be photocytes based on evidence have been found around the spine nerve plexus, mucous cells, and what are believed to be pigment cells. It has been found that luminescence is controlled by the animal's nervous system. Acetylcholine is able to stimulate the cells through nicotinic receptors. [8]

Amphipholis squamata

In Amphipholis squamata, bioluminescence has been observed to come from the spines emanating from the arms from photocytes within the spinal ganglia. Acetylcholine has been found to be able to stimulate the photocytes to produce light. [9]

Mollusks

It was discovered that bioluminescent snails are able to exercise a great deal of control over light emission, but the way in which they exercise control over it is still unknown. Phuphania have even been shown to be able to preserve their ability to produce light even after long periods of hibernation. It is currently unknown how these snails are able to maintain their ability to produce light for long periods of time, but theories have been proposed possibly relating it to the way certain fungi are able to maintain their bioluminescence. [10]

Other species of fish

Adrenaline stimulates photocytes to emit light for many species of fish. It is believed that sympathetic nervous impulses provide the stimulus that causes photocytes to emit light. [11]

Embryological development

Mnemiopsis leidyi

For Mnemiopsis leidyi , the ability to produce light is first observed upon the development of the plate cilia cells, and the bioluminescent cells found in the embryo share many characteristics with the photocytes observed in the adult organism. The M macromere lineage of cells are the ones that differentiate into photocytes, and they separate from other lineages of cells in the differential division. The subsequent maturation of the photocytes and intensification of light produced develop rapidly, occurring within ten hours of the first observed instance of bioluminescence. The egg of the organism contains two cytoplasmic regions: cortical and yolky, and the region of cytoplasm that daughter cells receive when the egg divides determine what they differentiate into. It was found that whether cortical cells exhibited bioluminescence or not was dependent on whether they inherited yolk in their cytoplasm with the cells containing yolk producing light and the cells without yolk not producing any light. [6]

Evolution of photocytes

Luciferins have been shown to be largely conserved among different species while luciferases show a greater degree of diversity. Eighty percent of the species that exhibit bioluminescence exist in aquatic habitats. [12]

Etmopterus spinax

Overall, the evolution of light producing cells (photocytes) is believed to have happened twice in sharks through convergence. Evidence suggests that the bioluminescent properties of the shark, Etmopterus spinax , came about as a mechanism of camouflage. It is thought that luminescence has other functions as well due to camouflage not being a logical explanation for the luminescence on the lateral sides of the shark. [13] Bioluminescence is believed to have only evolved in sharks among the cartilaginous fishes. The function of bioluminescence among sharks has not been fully ascertained. [12]

Evolution in fireflies

All five families of luminescent beetle, Phengodidae, Rhagophthalidae, Elateridae, Sinopyrophoridae, and Lampyridae are categorized into the Lampyroid clade. It has been determined that the luciferases and luciferin protein expressed in the photocytes of all species of firefly is homologous with that expressed in beetle species within the families Phengodidae, Rhagophthalidae, and Elateridae. In fact, every bioluminescent beetle species studied has been shown to use very similar mechanisms for light production in the photocyte. The beetle genus, Sinopyrophoridae, has been shown to exhibit bioluminescence although the exact mechanism is not known. It is believed that it shares homology with other genera of beetles however. The first time the entire genome of a bioluminescent beetle was determined was in 2017 with Pyrocoelia pectoralis, a species of firefly, and in 2018, three more species of bioluminescent beetle had their genomes sequenced. Biolumiescence in beetles has been shown to serve multiple purposes including the deterrence of predators and the attraction of mates. [2]

The variation in coloring among different species of firefly has been determined to be due to differences in the amino acid sequences of the luciferases expressed in their photocytes. Two luciferase genes have been identified in the genomes of fireflies. They are luc1-type and luc2-type. There is evidence that suggests that Luc1-type evolved from a gene duplication of the gene that encodes for acyl-CoA synthetase. It is hypothesized that the luciferase of click beetles evolved separately from that in fireflies being the result of two gene duplications of the acyl-CoA synthetase gene suggesting analogy instead of homology between the groups. Additional genes have been found to be related to the storage of luciferin. [2]

Amphiura filiformis

Bioluminescence in Amphiura filiformis and other species of sea star is widely believed to function in protection against predators. By attracting predators to one arm and losing the arm, the sea star is able to escape predation. [8]

Other species of fish

Fish generally use bioluminescence for camouflage to hide from predators. Endogenous photocytes are more commonly used for bioluminescence than other means like bacteria. Some fish may use the bioluminescence produced by their photocytes as a means of communication. [14]

Mollusks

Bioluminescence has only been observed in three classes of mollusks: Cephalopoda, Gastropoda, and Bivalvia. Bioluminescence is widely spread among cephalopods, but much rarer among the other classes of mollusk. Most species of bioluminescent mollusk that have been discovered are found in the ocean with the exception of the genera Latia and Quantula found in freshwater and terrestrial habitats respectively; however, more recent research has discovered luminescence in the Phuphania genus. It is hypothesized that terrestrial mollusks that use bioluminescence developed it as a strategy to deter predation. The green color emanated by the mollusk's photocytes is thought to be the most visible color to nocturnal predators. [10]

Structure and organelles

The mitochondria is believed to be important in controlling the supply of oxygen available for making light in fireflies. An increased rate of respiration decreases the intracellular oxygen concentration which reduces the amount available for light production. [4] The mitochondria of the photocyte exists near the perimeter of the cell while the peroxisome is typically found closer to the middle of the cell. [5] It is worth noting that not all bioluminescence in the firefly light organ occurs in the granules of the photocyte. Some fluorescent protein has been found to exist in the posterior region of the organ. [15]

Organelle targeting

It was found that the luciferase enzyme produced in fireflies is localized to the peroxisome within the photocytes. When mammalian cells were modified to produce the enzyme, it was found that they were targeted to the mammalian peroxisome as well. Because protein targeting to peroxisomes is not well understood, this finding is valuable for its potential to aid in the determination of peroxisome targeting mechanisms. If the cell produces a large amount of luciferase, some of the protein ends up in the cytoplasm. It is unknown what feature of the luciferase enzyme causes it to be targeted to the peroxisome since no particular protein sequences related to peroxisome targeting have been discovered. [16]

Arachnocampa luminosa

The photocyte of Arachnocampa luminosa was found to contain a circular nucleus, and large amounts of ribosomes, smooth endoplasmic reticulum, mitochondria, and microtubules. Instead of having photocyte granules, the photocytes of the organism were shown to undergo the luciferase reaction in their cytoplasm. The cells do not have a golgi apparatus or rough endoplasmic reticulum and were found to be 250 micrometers by 120 micrometers overall with a depth of 25 to 30 micrometers. [17]

Renilla köllikeri

The photocytes of Renilla köllikeri were found to have a diameter of eight to ten micrometers. The mitochondria of the photocytes were found to be very large with abnormally organized cristae surrounding the nucleus of the cell. The rough endoplasmic reticulum of the photocytes were found to exist close to the cell membrane. Several small vesicles, on the order of 0.25 micrometers, were found in the cell, and differently shaped granules containing diverse contents were also observed. [18]

Amphipholis squamata

The photocytes present in Amphipholis squamata have been found to contain a Golgi apparatus and rough endoplasmic reticulum. They have also been found to contain up to six different kinds of vesicles within their cytoplasm. [9]

Signal transduction

Signal transduction pathways in the photocyte of the firefly have been hypothesized to play a role in decreasing the activity of the mitochondria to make oxygen available for the production of light in fireflies. Because the neurons that control the lighting mechanism of the photocytes terminate at the tracheal cells instead of the photocytes, there must be some process that mediates the transference of the signal to them. Nitric oxide is believed to play this role partly due to the fact that it has already been implicated in a plethora of signaling roles in tissues among several, diverse clades of animal including insects. In fact, concentrations of nitric oxide on the order of 70 ppm have been found to result in flashing in fireflies, and carboxy-PTIO, a Nitric Oxide scavenger, has been shown to inhibit the response. Additionally, the tracheolar end organ was found to contain a high concentration of the enzyme nitric oxide synthase. Nitric oxide has been implicated with the action of decreasing respiration in the mitochondria. This effect on the mitochondria has been found to be influenced by surrounding light conditions with more light decreasing the action of nitric oxide on the mitochondria and less light increasing its action. In addition to ambient light, the light produced by the photocytes can also play an inhibitory role on the effect of nitric oxide. [4] The photocytes have been described as containing a vacuole that plays a role in signaling with the extracellular environment. [19] It has been found that octopamine triggers an adenylate cyclase which plays a role in triggering bioluminescence in the photocytes in fireflies. A reaction among D-luciferin, luciferase, and ATP has been implicated in the mechanism of light production in firefly photocytes. The fluorescent response was also found to be greater in basic conditions than in acidic conditions. [15]

Granules

The shape of the photocyte granules ranges from more round to more elliptical, and there are three types of photocyte granules. The bioluminescent reaction is confined to the granules. The granules range from 0.6 to 2.5 micrometers in the larval photocytes of Photuris pennsylvanica and between 2.5 and 4.5 micrometers in the adult photocytes of the Asiatic firefly. The size and shape of photocytes can exhibits a great deal of diversity among the species they are found in. The different types of granules have been observed together within individual photocytes. [19] The illumination of the photocytes is confined to the granules where the reaction occurs. [15]

Type I

The first type of photocyte granule has been found to contain between two and twelve microtubules. In addition, the matrix of the type I granule lacks a uniform shape or structure with ferritin distributed throughout. [19]

Type II

The second type of photocyte granule contains a large crystal surrounded by several small crystals within a matrix with no definite shape or form. T microtubules in the type two granules are associated with the face of the crystal. In addition ferritin has been found to be associated with the crystals. [19] Type II granules are hypothesized to exist in Amphiurus filiformis photocytes. [8]

Type III

The type III granules are characterized by the fact that they contain several tubules with thick walls. The ferritin present in the granules is associated with filament-like features contained in them. [19]

Identification techniques and culturing

Because the compounds that exhibit bioluminescence are typically fluorescent, fluorescence can be used to identify photocytes in organisms. [10]

Related Research Articles

<span class="mw-page-title-main">Bioluminescence</span> Emission of light by a living organism

Bioluminescence is the production and emission of light by living organisms. It is a form of chemiluminescence. Bioluminescence occurs widely in marine vertebrates and invertebrates, as well as in some fungi, microorganisms including some bioluminescent bacteria, and terrestrial arthropods such as fireflies. In some animals, the light is bacteriogenic, produced by symbiotic bacteria such as those from the genus Vibrio; in others, it is autogenic, produced by the animals themselves.

<span class="mw-page-title-main">Chemiluminescence</span> Emission of light as a result of a chemical reaction

Chemiluminescence is the emission of light (luminescence) as the result of a chemical reaction, i.e. a chemical reaction results in a flash or glow of light. A standard example of chemiluminescence in the laboratory setting is the luminol test. Here, blood is indicated by luminescence upon contact with iron in hemoglobin. When chemiluminescence takes place in living organisms, the phenomenon is called bioluminescence. A light stick emits light by chemiluminescence.

<span class="mw-page-title-main">Luciferase</span> Enzyme family

Luciferase is a generic term for the class of oxidative enzymes that produce bioluminescence, and is usually distinguished from a photoprotein. The name was first used by Raphaël Dubois who invented the words luciferin and luciferase, for the substrate and enzyme, respectively. Both words are derived from the Latin word lucifer, meaning "lightbearer", which in turn is derived from the Latin words for "light" (lux) and "to bring or carry" (ferre).

<span class="mw-page-title-main">Luciferin</span> Class of light-emitting chemical compounds

Luciferin is a generic term for the light-emitting compound found in organisms that generate bioluminescence. Luciferins typically undergo an enzyme-catalyzed reaction with molecular oxygen. The resulting transformation, which usually involves breaking off a molecular fragment, produces an excited state intermediate that emits light upon decaying to its ground state. The term may refer to molecules that are substrates for both luciferases and photoproteins.

<span class="mw-page-title-main">Foxfire</span> Fungal bioluminescence

Foxfire, also called fairy fire and chimpanzee fire, is the bioluminescence created by some species of fungi present in decaying wood. The bluish-green glow is attributed to a luciferase, an oxidative enzyme, which emits light as it reacts with a luciferin. The phenomenon has been known since ancient times, with its source determined in 1823.

<i>Noctiluca scintillans</i> Bioluminescent, marine dinoflagellate

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<span class="mw-page-title-main">Firefly luciferase</span>

Firefly luciferase is the light-emitting enzyme responsible for the bioluminescence of fireflies and click beetles. The enzyme catalyses the oxidation of firefly luciferin, requiring oxygen and ATP. Because of the requirement of ATP, firefly luciferases have been used extensively in biotechnology.

<span class="mw-page-title-main">Firefly luciferin</span> Chemical compound

Firefly luciferin is the luciferin, or light-emitting compound, used for the firefly (Lampyridae), railroad worm (Phengodidae), starworm (Rhagophthalmidae), and click-beetle (Pyrophorini) bioluminescent systems. It is the substrate of luciferase, which is responsible for the characteristic yellow light emission from many firefly species.

<span class="mw-page-title-main">Bioluminescence imaging</span>

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<span class="mw-page-title-main">Blackbelly lanternshark</span> Species of shark

The blackbelly lanternshark or lucifer shark is a shark of the family Etmopteridae found around the world in tropical and temperate seas at depths between 150 and 1,250 meters – the mesopelagic zone. Compared to other mesopelagic fish predators and invertebrates, the blackbelly lanternshark is thought to reside in shallower, more southern waters. E. lucifer can reach up to 47 centimeters in length and consumes mesopelagic cephalopods, fish, and crustaceans. Blackbelly lanternsharks are bioluminescent, using hormone controlled mechanisms to emit light through ventral photogenic organs called photophores and are presumed to be ovoviviparous. The blackbelly lanternshark has been classified as "Not Threatened" within the New Zealand Threat Classification System.

<span class="mw-page-title-main">Slendertail lanternshark</span> Species of shark

The slendertail lanternshark or Moller's lanternshark is a shark of the family Etmopteridae found in the western Indian Ocean between latitudes 34°N and 46°S at depths between 250 and 860 m. It can grow up to 46 cm in length.

<span class="mw-page-title-main">Splendid lanternshark</span> Species of shark

The splendid lanternshark is a shark of the family Etmopteridae found in the western Pacific at depths between 120 and 210 m. Through the classification of Etmopterus species into several clades based on the positioning of their bioluminescent photophores, the splendid lanternshark can be considered a member of the Etmopterus pusillus clade.

In enzymology, an Oplophorus-luciferin 2-monooxygenase, also known as Oplophorus luciferase is a luciferase, an enzyme, from the deep-sea shrimp Oplophorus gracilirostris [2], belonging to a group of coelenterazine luciferases. Unlike other luciferases, it has a broader substrate specificity [3,4,6] and can also bind to bisdeoxycoelenterazine efficiently [3,4]. It is the third example of a luciferase to be purified in lab [2]. The systematic name of this enzyme class is Oplophorus-luciferin:oxygen 2-oxidoreductase (decarboxylating). This enzyme is also called Oplophorus luciferase.

<span class="mw-page-title-main">Renilla-luciferin 2-monooxygenase</span>

Renilla-luciferin 2-monooxygenase, Renilla luciferase, or RLuc, is a bioluminescent enzyme found in Renilla reniformis, belonging to a group of coelenterazine luciferases. Of this group of enzymes, the luciferase from Renilla reniformis has been the most extensively studied, and due to its bioluminescence requiring only molecular oxygen, has a wide range of applications, with uses as a reporter gene probe in cell culture, in vivo imaging, and various other areas of biological research. Recently, chimeras of RLuc have been developed and demonstrated to be the brightest luminescent proteins to date, and have proved effective in both noninvasive single-cell and whole body imaging.

<i>Photinus pyralis</i> Species of beetle

Photinus pyralis, also known by the common names the common eastern firefly or big dipper firefly, and sometimes called a "lightning bug", is a species of flying beetle. An organ on its abdomen is responsible for its light production. It is the most common species of firefly in North America, and is typically found east of the Rocky Mountains. Photinus fireflies are often confused with fireflies of the similar-sounding genus, Photuris, which are also found in North America.

<i>Vargula hilgendorfii</i> Species of seed shrimp

Vargula hilgendorfii, sometimes called the sea-firefly and one of three bioluminescent species known in Japan as umi-hotaru (海蛍), is a species of ostracod crustacean. It is the only member of genus Vargula to inhabit Japanese waters; all other members of its genus inhabit the Gulf of Mexico, the Caribbean Sea, and waters off the coast of California. V. hilgendorfii was formerly more common, but its numbers have fallen significantly.

<span class="mw-page-title-main">John Woodland Hastings</span>

John Woodland "Woody" Hastings, was a leader in the field of photobiology, especially bioluminescence, and was one of the founders of the field of circadian biology. He was the Paul C. Mangelsdorf Professor of Natural Sciences and Professor of Molecular and Cellular Biology at Harvard University. He published over 400 papers and co-edited three books.

<span class="mw-page-title-main">Dinoflagellate luciferase</span>

Dinoflagellate luciferase (EC 1.13.12.18, Gonyaulax luciferase) is a specific luciferase, an enzyme with systematic name dinoflagellate-luciferin:oxygen 132-oxidoreductase.

<span class="mw-page-title-main">Bioluminescent bacteria</span>

Bioluminescent bacteria are light-producing bacteria that are predominantly present in sea water, marine sediments, the surface of decomposing fish and in the gut of marine animals. While not as common, bacterial bioluminescence is also found in terrestrial and freshwater bacteria. These bacteria may be free living or in symbiosis with animals such as the Hawaiian Bobtail squid or terrestrial nematodes. The host organisms provide these bacteria a safe home and sufficient nutrition. In exchange, the hosts use the light produced by the bacteria for camouflage, prey and/or mate attraction. Bioluminescent bacteria have evolved symbiotic relationships with other organisms in which both participants benefit each other equally. Bacteria also use luminescence reaction for quorum sensing, an ability to regulate gene expression in response to bacterial cell density.

<span class="mw-page-title-main">Scintillon</span>

Scintillons are small structures in cytoplasm that produce light. Among bioluminescent organisms, only dinoflagellates have scintillons.

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