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Luminescence of Higher Mushrooms

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Luminescence of Higher Mushrooms Journal of Siberian Federal University. Biology 4 (2012 5) 331-351 ~ ~ ~ УДК 577.332.23: 539.199 Luminescence of Higher Mushrooms Vladimir S. Bondara,b*, УДК 577.332.23: 539.199 Osamu Shimomuraa,c and Josef I. Gitelsona,b a Luminescence of Higher Mushrooms Siberian Federal University, 79 Svobodny, Krasnoyarsk, 660041 Russia b Institute of Biophysics SB RAS, Vladimir S. Bondara,b,*, Osamu Shimomuraa,c and Josef I. Gitelson50/50a,b Akademgorodok, Krasnoyarsk, 660036 Russia c a Marine Biological Laboratory, Woods Hole, Institute of Fundamental Biology and Biotechnology, Siberian Federal University, 79 Massachusetts, 02543 United States of America 1 Svobodny, Krasnoyarsk, 660041 Russia bInstitute of Biophysics SB RAS, 50/50 Akademgorodok, Krasnoyarsk,Received 66003613.12.2012, Russia received in revised form 20.12.2012, accepted 27.12.2012 c Marine Biological Laboratory, Woods Hole, Massachusetts,The review 02543 highlights United theStates results of Americaof experimental studies on fungal luminescence carried out during last two centuries. Present concepts on the luminescent system and light emission mechanism in higher fungi are discussed. *Corresponding author E-mail address: [email protected] Keywords: higher mushrooms, bioluminescence, chemiluminescence, luciferase, luciferin, emitter. Unique position the kingdom of mushrooms holds in the living nature was sagaciously foretold by French botanist and mycologist Sebastien Vaillant whose words are given in the epigraph of this paper. Fabulous foresight at the turn of the XVIIth and XVIIIth centuries when nothing was known about biochemistry, not to mention genetics. Yet, further development of biology proves equidistance of the kingdom of mushrooms from both animals and plants. But traditions die hard and up to now mycology is «Fungi – are the devil product that disturbs the general harmony «Fungiof nature, – are theto confusedevil product the that most studied in universities in the course of general disturbs the general harmony of nature, botany. talented researchers and get of young botanists in despair» (Vaillant Sébastien, 1669-1722). to confuse the most talented researchers The mechanism of bioluminescence in and get of young botanists in despair» fungi, the knowledge of which is reviewed in this The review highlights the results of experimental studies on fungal luminescence(Vaillant Sébastien, carried 1669-1722).out work, also proves their unique position. Fungi during last two centuries. Present concepts on the luminescent system and light emission * Corresponding author E-mail address: [email protected] mechanism in higher fungi are discussed. 1 © Siberian Federal University. All rights reserved Keywords: higher mushrooms, bioluminescence, chemiluminescence, luciferase, luciferin, – 331 – emitter. Unique position the kingdom of mushrooms holds in the living nature was sagaciously foretold by French botanist and mycologist Sebastien Vaillant whose words are given in the epigraph of this paper. Fabulous foresight at the turn of the XVIIth and XVIIIth centuries when nothing was known about biochemistry, not to mention genetics. Yet, further development of biology proves equidistance of the kingdom of mushrooms from both animals and plants. But 1 Figures: Vladimir S. Bondar, Osamu Shimomura… Luminescence of Higher Mushrooms Fig. 1. Emission of visible light by mushrooms: А – Mycena lampadis; B – Filoboletus sp.; C – Mycena sp.; D, E, F – Panellus stipticus; G, H – Omphalotus sp.; I – Fig.Neonothopanus 1. nambi. Photographs (A – H) – from official sites of National Geographic (http://news.nationalgeographic.com/news/) and Flikr® from Yahoo (http://www. flickr.com /); photo (I) was kindly provided by Vietnamese researcher Dao Thi Van (Bio-Lumi Co., Ltd., Ho Chi Minh City, Vietnam) 3 share bioluminescence capability with animals Elder noted that luminescent white mushrooms and bacteria, however, 2the deeper the insight into with sweetish taste and exhibiting pharmacological the mechanism of this amazing phenomenon the effect can be found on rotting trees. G.E. Rumph more obvious is its fundamental distinction in wrote in «Herbarium Amboiense», that residents mushrooms from the 1luminescence mechanism of Moluccas (Indonesia) illuminated their way in of animals and plants.light (arb. emission un.) a dark forest by fruiting bodies of bioluminescent Bioluminescence of fungi, emission of light mushrooms (quote from Harvey, 1957). Harvey visible with unaided eye0 (Fig. 1), has been known (1957) noted that on the one hand the aboriginals 400 500 600 700 down the ages. Several authors (Johnson, Haneda of Micronesia used luminescent mushrooms wavelength (nm) 1966; Shimomura, 2006) note, that according to as decorations for ritual dances to paint their Harvey, this phenomenon was described as early faces to intimidate enemies, on the other hand Fig. 2. as by Aristotle (fourth century BC) and Pliny the luminous mushrooms were frequently destroyed Elder (first century AC) in «Historia Naturalis» because to find them was considered an ill omen. (Harvey, 1952, 1957). Describing luminescence Emotions of people who saw for the first time the of rotting tree Aristotle called this phenomenon mushrooms glow is anyone’s guess. Surviving «shining wood» and «fox fire», while Pliny the20 rave records of seafarers of Ancient times speak – 332 – Vladimir S. Bondar, Osamu Shimomura… Luminescence of Higher Mushrooms of the mind-bending effect of luminescence of heat – light goes down in vacuum, in hydrogen marine organisms. The emotional impact of and in carbon dioxide; 2 – luminescence does luminescence of mushrooms was probably not not depend on humidity, temperature, or external less (Fig. 1). light, and does not become brighter in pure oxygen Aristotle’s and Pliny the Elder’s works and (quote from Harvey, 1957). J. Schmitz made a reports of botanists about wide occurrence of detailed description of rhizomorphs; F. Ludwig luminescent mushrooms notwithstanding, for presented his dissertation on the luminescence of a long time researchers focused their efforts mushrooms and wood; H. Molisсh published in on luminescence of rotting trees, but not the 1904 a monograph on luminous plants (quote by mushrooms, as they are. For instance, well Yachevsky, 1933). known is the work by Robert Boyle (1668), who It should be mentioned that in the two recent used an air pump to demonstrate necessity of air centuries a considerable number of the species of for wood to glow. Therefore, the most important luminous mushroom were found; most of them discoveries pertaining directly to bioluminescence belong to basidiomycetes class (Shimomura, of mushrooms were made by researchers much 2006). By now luminous mushrooms have been later – the first half of the XIXth century. Scientific found in North and South America, Europe, Asia, works of this period give some insight into the Australia, and Africa. The list keeps steadily way in which the views of researchers studying growing because more and more new species are luminescence of wood and trying to understand found, specifically in the subtropical and tropical the cause of this phenomenon transformed. J.F. zones of the globe where natural conditions are Heller, Professor of the University of Vienna, was most favorable for their habitation. While in the among the first who associated luminescence of first half of the XXth century A.A. Yachevsky rotting wood with presence of mushrooms; (1933) reported only 28 species of luminous thorough examinations by von Derschau et al. mushrooms, by the end of the century their made possible to conclude that luminescence number had grown to 40 species (Wassink, 1978; of wood is associated with presence of fungal Herring, 1994). Modern methods of identifying mycelium (von Derschau’s letter was published biological objects allowed Desjardin et al. (2008) in 1823 by the German botanist T.F.L. Nees to attribute about 70 species of basidiomycetes to von Esenbeck); Conrade Gesner, Francis Bacon luminous mushrooms. Further studies of fungal and Thomas Bartholin left their records about bioluminescence made possible to put in the list glowing soil (quote by Harvey, 1952, 1957). already 80 species of luminous mushrooms, not Luminescence of mushrooms was observed in including synonyms (Vydryakova et al., 2009). 1815 by P. Heinrich; J.F. Heller noted in 1853 that Recently seven more new species of luminous luminescence is a biological process (quote by mushrooms were found; the authors attributed Yachevsky, 1933). them to Mycena family (Desjardin et al., 2010). The pioneer works of the first half of the Even though mushroom bioluminescence XIXth century mentioned above opened the way has been studied out for many years, research and largely facilitated further studies of fungal is focused on three main directions. They are: luminescence. In 1855 J.H. Fabre experimentally to develop methods of cultivating luminous established basic parameters of mushroom mushrooms under laboratory conditions (Endo bioluminescence and formulated two important et al., 1970; Bermudes et al., 1990; Weitz et al., conclusions: 1 – luminescence is not attended by 2001; Mendes et al., 2008; Dao, 2009), to study – 333 – Figures: Fig. 1. Vladimir S. Bondar, Osamu Shimomura… Luminescence of Higher Mushrooms 3 2 1 light (arb. emission un.) 0 400 500 600 700 wavelength (nm) Fig. 2. Bioluminescence spectrum of N. nambi myceliumFig. in2. vivo (Bondar et al., 2011) molecular organization of the luminescent and before that period, it practically does not system and the mechanisms
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