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BIOLUMINESCENCE, the NATURE of the LIGHT BIOLUMINESCENCE, the NATURE of the LIGHT “Experiment, is the interrogation of Nature” Robert Boyle 1665 FROM: Robert Boyle. New Experiments Physico-Mechanicall: Touching the Spring of the Air and its Effects (1660) John Lee The University of Georgia 2017 This is the fifth update of this book first deposited in 2014 in the digital library collection Atheneum@UGA: http://athenaeum.libs.uga.edu/xmlui/ The most recent edition can be downloaded here: http://hdl.handle.net/10724/20031 This work is for educational and non-commercial use only. The book in total may be freely downloaded. Parts may be freely copied for use with attribution. This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license. http://creativecommons.org/licenses/by/4.0/ http://www.bmb.uga.edu/directory/john-lee National Library of Medicine http://www.ncbi.nlm.nih.gov/nlmcatalog/?term=101675046 April 2017 CONTENTS 1. History. Bioluminescence and the Theory of Light (1) 2. Bioluminescence to 1950. Biology, Biochemistry, and Physics (9) 3. Bioluminescence in the 1950s. Johns Hopkins and Princeton Universities, and Oak National Laboratory (15) 4. Bioluminescence Kinetics (23) 5. Quantum Yields (46) 6. Quantitative Molecular Spectroscopy (56) 7. Chemiluminescence (74) 8. Marine Bioluminescence and Coelenterazine (94) 9. Bioluminescence of Beetles (108) 10. Bacterial Bioluminescence (122) 11. Dinoflagellates: “Phosphorescence” in the Sea (127) 12. Structural Biology (133) 13. The Antenna Proteins. Bioluminescence FRET (163) 14. Computational Bioluminescence (178) 15. In Depth (187) 16. Figure Attributions (201) 17. Afterword (210) 1 1. History. Bioluminescence and the Theory of Light “And the angel of the LORD appeared unto him in a flame of fire out of the midst of a bush; and he looked, and, behold, the bush burned with fire, and the bush was not consumed.” EXODUS 3:2. Among many speculations about Moses and the “burning bush” one is that the “flame” was from an infection of bioluminescent fungi on the decaying leaves, meaning that Moses should be credited with the first published report (~1450 BCE) of a bioluminescence! Another thousand years passed before the existence of records of the more reliable observations by the natural philosophers of Ancient Greece, many having an intense interest in the nature of visible light, and another two thousand years before Isaac Newton’s postulate of the corpuscular theory of light. It was evident to the Ancients that light took many forms, a hot light from the sun, fire, and oil lamps, light without any warmth from the heavenly bodies, and the cold luminescence emanating from many living creatures. Euclid (Optics, 300 BCE) disputed an earlier theory that light rays came from the eye, instead insisting that light originated in the object itself, based on his observations that light traveled in straight lines and of the laws of reflection. In contrast to the highly illuminated environment we inhabit at this present day, even until the last few hundred years most of humanity lived at least a third of the day in darkness. The result of efficient dark adaptation of the eye was to allow ready detection of the self- luminescence from the many terrestrial forms of bioluminescence, fireflies and glow-worms, rotting wood, and of the light from agitated sea-water as well as from many marine creatures. Written reports remained fragmentary up till the time of Aristotle (384-322 BCE), who was the first to recognize the self-luminosity of organisms and that it was not accompanied by heat. Aristotle wrote about the glow from dead fish or flesh now known to be from an infection by bioluminescent bacteria, and the light generated on disturbance of sea-water, and of fireflies and glow-worms. Pliny the Elder (23-79 CE) in his Naturalis Historia, wrote quite detailed descriptions of many bioluminescent animals: glowworms and fireflies, the luminous mollusk Pholas dactylus (a Roman delicacy), the purple jellyfish Pelagia noctilus common in the Mediterranean, the lantern fish, and the fungi, glowing wood and mushrooms (Fig. 1.1). In the period following the fall of the Roman Empire (ca. 500 CE) very few new reports of bioluminescent organisms can be found. Even though progress in scientific investigation continued elsewhere, in Arabia, India, and China, little interest in the theory of light or particularly the nature of animal light, seems to be evident from any written records. Perhaps the history of science in these areas has not received sufficient attention, even in the scholarly work on the History of Science in China by Joseph Needham. 2 Figure 1.1. Some bioluminescent organisms described by Pliny the Elder (23-79 CE). The book De Animalibus published in1478, was a collection of the works of Albertus Magnus (1206-1280 CE), a German monk, but although he described and cataloged many luminous species, not much was added to Pliny the Elder’s earlier list. Of particular interest, Magnus claimed that it was possible to make extracts of fireflies, Liquor Lucidus that produced a permanent luminescence. Later investigators in following centuries were unable to reproduce Magnus’s results, so cast doubt on his discovery. We have to leave open the attribution of the first in vitro extract of bioluminescence therefore, until almost 800 years later, until the experiments of Raphaël Dubois in Paris. The time of the Renaissance in Europe, in the few hundred years before the end of the 15th Century, saw a revival of learning as well as an increase in maritime exploration and trade. Voyagers brought back reports of “burning seas” probably the phenomenon now called “milky seas” suggested to be due the bioluminescent marine bacteria. Christopher Columbus (1492) referred to mysterious lights in the sea nearby San Salvador, probably from the marine worms Odontosyllis known to inhabit these Caribbean waters. Oviedo (1478-1557) in Spain, published extensively on the natural history of the New World. He described the elaterid (“click”) beetle Pyrophorus, bioluminescent caterpillars, and railroad worms (Phrixothrix) (Fig. 1.2). Tropical fireflies in the East Indies were also seen by Sir Francis Drake (1540- 1596). Conrad Gesner (1516-1565), Professor of Natural History and Medicine in Zurich, is credited with writing the first book devoted to luminescence, De Lunariis (1555). This book was a collection of all observations going back to ancient times, of bioluminescent animals and also of luminous stones. He listed several marine bioluminescent species and the terrestrial forms, fireflies, caterpillars, luminous wood and flesh. For scholars, the 16th Century was a period of collecting and reporting of natural phenomena such as bioluminescence, with little attempt at explanation. The value of “experimentation” was not yet ready to be realized. 3 Firefly Phrixothrix Pyrophorus Figure 1.2. Representatives of the three families of bioluminescent beetles: Firefly, railroad worm, click beetle. (V.R.Viviani). The 17th Century is known as the age of the “Science Revolution”. Up till 1600 CE, as a consequence of the increase in exploration and commerce, there was a demand for reliable and predictive knowledge that required development of an objective methodology for discovery. Also, there were advances in technology, such as the invention of the telescope and the microscope, enabling the astronomical discoveries of Galileo (1564-1642) and of van Leeuwenhoek (1632-1723) in microbiology. The air pump, improved by Boyle (1627-1691) and his able assistant Hooke (1635-1703), led to landmark observations in bioluminescence and many related phenomena. The foundations of the scientific method at this time were laid by the writings of Sir Francis Bacon (1561-1626) in England and Renee Descartes (1596-1650) in France. Bacon proposed that true knowledge is to be obtained by first collecting a sufficient number of carefully observed and verifiable particulars, or instances. Then one could propose a modest generalization or axiom, from which a direction for collecting more observations would be indicated. He emphasized that it was important to find new instances whereby the axiom could be refuted, because this would suggest that a better axiom was needed. Bacon recorded observations of triboluminescence for example but never developed any theory of light, indeed in the Baconian system, establishing hypotheses is not considered so important. In contrast, the doctrine espoused by Descartes was that a Grand Theory was essential in Science, from which deduction from such a grand Principle is used to arrive at a particular instance. Descartes did propose a theory of light, first he dismissed the idea that space could be a vacuum, instead he imagined it to be a plenum of contiguous particles, all jostling and crowded together. He thus deduced that light originated from the friction of particles rubbing together as observed for triboluminescence, and that light is transmitted by one particle pushing against the next. Light from sea-water he proposed, arose from vigorous disturbance by the oars of the boat, and the light from fish due to particles of salt penetrating the pores. Workers of the French school followed Descarte’s generalization and put forward similar explanations for other bioluminescence phenomena. By the end of the 17th Century the Theory of Light had divided into opposing views, the wave theory of Hooke and Huygens, and that light consisted of particles, an idea more associated with Newton (1642-1727) than Descartes. Due mainly to the dominant reputation of Newton, 4 his corpuscular theory remained unchallenged for almost 150 years, when it was clearly incompatible with the diffraction experiments of Young and the work of Fresnel. Kircher (1602-1680), a German Jesuit priest, applying the Baconian principle, collected and tabulated many new observations of bioluminescent phenomena. He noted that in fireflies, the light would dim on handling the insect, and then reappear if left alone.
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