Bioluminescence
Bioluminescence is the production of light by an organism as the result of a chemiluminescence reaction. It occurs in a wide variety of organisms, including marine vertebrates and invertebrates, terrestrial arthropods such as fireflies, some fungi, and microorganisms such as some bacteria and dinoflagellates. 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. Bioluminescence has evolved independently at least 94 times, first emerging in octocorals some 540 million years ago.
In most cases, the principal chemical reaction in bioluminescence involves the reaction of a substrate called luciferin and an enzyme, called luciferase. Because these are generic names, luciferins and luciferases are often distinguished by the species or group, e.g. firefly luciferin or cypridina luciferin. In all characterized cases, the enzyme catalyzes the oxidation of the luciferin resulting in excited state oxyluciferin, which is the light emitter of the reaction. Upon their decay to the ground state they emit visible light.
In some species, the luciferase requires other cofactors, such as calcium or magnesium ions, and sometimes also the energy-carrying molecule adenosine triphosphate. In evolution, luciferins vary little: one in particular, coelenterazine, is found in 11 different animal phyla, though in some of these, the animals obtain it through their diet. Conversely, luciferases vary widely between different species. Bioluminescence has arisen over 40 times in evolutionary history.
Both Aristotle and Pliny the Elder mentioned that damp wood sometimes gives off a glow. Many centuries later Robert Boyle showed that oxygen was involved in the process, in wood, fish, and glowworms. It was not until the late nineteenth century that bioluminescence was properly investigated. The phenomenon is widely distributed among animal groups, especially in marine environments. On land it occurs in fungi, bacteria and some groups of invertebrates, including insects.
The uses of bioluminescence by animals include counterillumination camouflage, mimicry of other animals, for example to lure prey, and signaling to other individuals of the same species, such as to attract mates. In the laboratory, luciferase-based systems are used in genetic engineering and biomedical research.
History
Before the development of the safety lamp for use in coal mines, dried fish skins were used in Britain and Europe as a weak source of light. This experimental form of illumination avoided the necessity of using candles which risked sparking explosions of firedamp. In 1920, the American zoologist E. Newton Harvey published a monograph, The Nature of Animal Light, summarizing early work on bioluminescence. Harvey notes that Aristotle mentions light produced by dead fish and flesh, and that both Aristotle and Pliny the Elder mention light from damp wood. He records that Robert Boyle experimented on these light sources, and showed that both they and the glowworm require air for light to be produced. Harvey notes that in 1753, J. Baker identified the flagellate Noctiluca "as a luminous animal" "just visible to the naked eye", and in 1854 Johann Florian Heller identified strands of fungi as the source of light in dead wood.James Hingston Tuckey, in his posthumous 1818 Narrative of the Expedition to the Zaire, described catching the animals responsible for luminescence. He mentions pellucida, crustaceans, and cancers. Under the microscope he described the "luminous property" to be in the brain, resembling "a most brilliant amethyst about the size of a large pin's head".
Charles Darwin noticed bioluminescence in the sea, describing it in his Journal:
While sailing in these latitudes on one very dark night, the sea presented a wonderful and most beautiful spectacle. There was a fresh breeze, and every part of the surface, which during the day is seen as foam, now glowed with a pale light. The vessel drove before her bows two billows of liquid phosphorus, and in her wake she was followed by a milky train. As far as the eye reached, the crest of every wave was bright, and the sky above the horizon, from the reflected glare of these livid flames, was not so utterly obscure, as over the rest of the heavens.
Darwin also observed a luminous "jelly-fish of the genus Dianaea", noting that: "When the waves scintillate with bright green sparks, I believe it is generally owing to minute crustacea. But there can be no doubt that very many other pelagic animals, when alive, are phosphorescent." He guessed that "a disturbed electrical condition of the atmosphere" was probably responsible. Daniel Pauly comments that Darwin "was lucky with most of his guesses, but not here", noting that biochemistry was too little known, and that the complex evolution of the marine animals involved "would have been too much for comfort".
File:Aequorea4.jpg|thumb|Osamu Shimomura isolated the photoprotein aequorin and its cofactor coelenterazine from the crystal jelly Aequorea victoria in 1961.
Bioluminescence attracted the attention of the United States Navy in the Cold War, since submarines in some waters can create a bright enough wake to be detected; a German submarine was sunk in the First World War, having been detected in this way. The Navy was interested in predicting when such detection would be possible, and hence guiding their own submarines to avoid detection.
Among the anecdotes of navigation by bioluminescence is one recounted by the Apollo 13 astronaut Jim Lovell, who as a Navy pilot had found his way back to his aircraft carrier USS Shangri-La when his navigation systems failed. Turning off his cabin lights, he saw the glowing wake of the ship, and was able to fly to it and land safely.
The French pharmacologist Raphaël Dubois carried out work on bioluminescence in the late nineteenth century. He studied click beetles and the marine bivalve mollusc Pholas dactylus. He refuted the old idea that bioluminescence came from phosphorus, and demonstrated that the process was related to the oxidation of a specific compound, which he named luciferin, by an enzyme. He sent Harvey siphons from the mollusc preserved in sugar. Harvey had become interested in bioluminescence as a result of visiting the South Pacific and Japan and observing phosphorescent organisms there. He studied the phenomenon for many years. His research aimed to demonstrate that luciferin, and the enzymes that act on it to produce light, were interchangeable between species, showing that all bioluminescent organisms had a common ancestor. However, he found this hypothesis to be false, with different organisms having major differences in the composition of their light-producing proteins. He spent the next 30 years purifying and studying the components, but it fell to the young Japanese chemist Osamu Shimomura to be the first to obtain crystalline luciferin. He used the sea firefly Vargula hilgendorfii, but it was another ten years before he discovered the chemical's structure and published his 1957 paper Crystalline Cypridina Luciferin. Shimomura, Martin Chalfie, and Roger Y. Tsien won the 2008 Nobel Prize in Chemistry for their 1961 discovery and development of green fluorescent protein as a tool for biological research.
Harvey wrote a detailed historical account on all forms of luminescence in 1957. An updated book on bioluminescence covering also the twentieth and early twenty-first century was published recently.
Evolution
In 1932 E. N. Harvey was among the first to propose how bioluminescence could have evolved. In this early paper, he suggested that proto-bioluminescence could have arisen from respiratory chain proteins that hold fluorescent groups. This hypothesis has since been disproven, but it did lead to considerable interest in the origins of the phenomenon. Today, the two prevailing hypotheses are those put forth by Howard Seliger in 1993 and Rees et al. in 1998.Seliger's theory identifies luciferase enzymes as the catalyst for the evolution of bioluminescent systems. It suggests that the original purpose of luciferases was as mixed-function oxygenases. As the early ancestors of many species moved into deeper and darker waters natural selection favored the development of increased eye sensitivity and enhanced visual signals. If selection were to favor a mutation in the oxygenase enzyme required for the breakdown of pigment molecules it could have eventually resulted in external luminescence in tissues.
Rees et al. use evidence gathered from the marine luciferin coelenterazine to suggest that selection acting on luciferins may have arisen from pressures to protect oceanic organisms from potentially deleterious reactive oxygen species. The functional shift from antioxidation to bioluminescence probably occurred when the strength of selection for antioxidation defense decreased as early species moved further down the water column. At greater depths exposure to ROS is significantly lower, as is the endogenous production of ROS through metabolism.
While popular at first, Seliger's theory has been challenged, particularly on the biochemical and genetic evidence that Rees examines. What remains clear, however, is that bioluminescence has evolved independently at least 40 times. Bioluminescence in fish began at least by the Cretaceous period. About 1,500 fish species are known to be bioluminescent; the capability evolved independently at least 27 times. Of these, 17 involved the taking up of bioluminous bacteria from the surrounding water while in the others, the intrinsic light evolved through chemical synthesis. These fish have become surprisingly diverse in the deep ocean and control their light with the help of their nervous system, using it not just to lure prey or hide from predators, but also for communication.
All bioluminescent organisms have in common that the reaction of a "luciferin" and oxygen is catalyzed by a luciferase to produce light. McElroy and Seliger proposed in 1962 that the bioluminescent reaction evolved to detoxify oxygen, in parallel with photosynthesis.
Bioluminescence has evolved independently at least 94 times, first emerging in octocorals some 540 million years ago. It has evolved independently 27 times within the ray-finned fishes. The oldest of these appear to be Stomiiformes and Myctophidae. In sharks, it has evolved only once.
Genomic analysis of octocorals indicates that their ancestor was bioluminescent as long as 540 million years ago.