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Brazilian Bioluminescent Beetles: Reflections on Catching Glimpses of Light in the Atlantic Forest and Cerrado

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Brazilian Bioluminescent Beetles: Reflections on Catching Glimpses of Light in the Atlantic Forest and Cerrado Anais da Academia Brasileira de Ciências (2018) 90(1 Suppl. 1): 663-679 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201820170504 www.scielo.br/aabc | www.fb.com/aabcjournal Brazilian Bioluminescent Beetles: Reflections on Catching Glimpses of Light in the Atlantic Forest and Cerrado ETELVINO J.H. BECHARA and CASSIUS V. STEVANI Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, 05508-000 São Paulo, SP, Brazil Manuscript received on July 4, 2017; accepted for publication on August 11, 2017 ABSTRACT Bioluminescence - visible and cold light emission by living organisms - is a worldwide phenomenon, reported in terrestrial and marine environments since ancient times. Light emission from microorganisms, fungi, plants and animals may have arisen as an evolutionary response against oxygen toxicity and was appropriated for sexual attraction, predation, aposematism, and camouflage. Light emission results from the oxidation of a substrate, luciferin, by molecular oxygen, catalyzed by a luciferase, producing oxyluciferin in the excited singlet state, which decays to the ground state by fluorescence emission. Brazilian Atlantic forests and Cerrados are rich in luminescent beetles, which produce the same luciferin but slightly mutated luciferases, which result in distinct color emissions from green to red depending on the species. This review focuses on chemical and biological aspects of Brazilian luminescent beetles (Coleoptera) belonging to the Lampyridae (fireflies), Elateridae (click-beetles), and Phengodidae (railroad-worms) families. The ATP- dependent mechanism of bioluminescence, the role of luciferase tuning the color of light emission, the “luminous termite mounds” in Central Brazil, the cooperative roles of luciferase and superoxide dismutase against oxygen toxicity, and the hypothesis on the evolutionary origin of luciferases are highlighted. Finally, we point out analytical uses of beetle bioluminescence for biological, clinical, environmental, and industrial samples. Key words: Coleoptera, bioluminescence, luciferase, luciferin, luminous termitary, oxidative stress. INTRODUCTION (oxyluciferin*), which decays to the ground state emitting fluorescence (Shimomura 2012, Wilson Bioluminescence is defined as visible and cold and Hastings 2013). Thus, bioluminescence results light emission by living organisms. It results from from conversion of chemical energy into photons: the oxidation of a substrate called luciferin by molecular oxygen catalyzed by an enzyme named Luciferin + O2 (luciferase) → Oxyluciferin* → luciferase, leading to a singlet excited-state product Oxyluciferin + Light Correspondence to: Etelvino José Henriques Bechara E-mail: [email protected] This review concerns about 30 years of * Contribution to the centenary of the Brazilian Academy of investigation on several species of Brazilian Sciences. bioluminescent beetles (Coleoptera), mainly An Acad Bras Cienc (2018) 90 (1 Suppl. 1) 664 ETELVINO J.H. BECHARA and CASSIUS V. STEVANI click-beetles (Elateridae) and railroad-worms Yet the moon turned to the sun, full of spite: (Phengodidae) found in the Brazilian Atlantic “Wretch! I would have thy clarity overwhelming Forest and the Cerrado biome. During the rainy Shining immortal, all light joined in one!” season, after sunset, bright and multicolored light Replied the Sun, his shining crown bending: flashes emitted by flying beetles (Coleoptera) offer “Weary am I of this halo of luminous sky a magnificent visual spectacle (Bechara 1988, This light and boundless canopy weighs heavy. Bechara and Viviani 2015). Not surprisingly, Oh, that I were born a humble firefly!” how and why these worldwide distributed insects emanate intense and cold light are questions that Vicious Circle, Machado de Assis have awakened the curiosity of ordinary people, (Courtesy free translation by Clara Allain) writers, philosophers and scientists since ancient In fact, an attentive onlooker would soon realize times (Harvey 1957). Impressed by the intense that the beetles, swirling in their glimmering cloud, flashes of light sparked by the firefly at night, are caught up in their nuptial flight. Afterwards, Machado de Assis, a renowned Brazilian writer the insects pose on leaves and grass for copulation. wrote the sonnet Círculo Vicioso (Vicious Circle) In Brazil, the occurrence of fireflies and other where a whispering chain of firefly, star, moon, and luminous insects was first registered by Gabriel de the sun envy the brighter one, and finally the sun, Souza in 1587 in a document to Felipe I, King of feeling itself too radiant and hot, wishes to be a Portugal and Spain, describing “mamoás” (fireflies) simple firefly. The sonnet ‘jealous’ insect aspires and “buijejas” (probably, railroad-worms) so called to be able to chemically produce as much energy by the Amerindians of the State of Bahia (Moraes as the nuclear forces of the stars, being orders of 1940). Fireflies (Lampyridae), click-beetles magnitude higher. (Elateridae) and railroad-worms (Phengodidae) constitute the three most abundant families of Dancing in the air, moaned a restless firefly: luminescent coleopterans in Brazil (Fig. 1). “Oh, would that I could be that star so yellow Until present days, elucidation of the Shining in the everlasting blue, as a candle biochemical mechanism of a given luminescent mellow!” organism, be it a fly (Viviani et al. 2002) or a But the star gazed at the moon with envy high: mushroom (Oliveira and Stevani 2009), frequently “If only I could copy thy wondrous silver light, employs the preparation of a “hot” extract by heat- That from column Greek to Gothic window-case induced enzyme denaturation: the initial step of the Hath gazed with longing on my beloved’s face!” basic protocol long established by Raphael Dubois Figure 1 - Photographs of a firefly (Macrolampis omissa) (a), a click-beetle (Pyrophorus sp.) (b), and a railroad-worm (Phrixothrix hirtus) (c). An Acad Bras Cienc (2018) 90 (1 Suppl. 1) CHEMISTRY AND BIOLOGY OF BEETLE BIOLUMINESCENCE 665 (1886) when studying the basic ingredients for but glowing with the increase of bacterial density light emission by a click-beetle, formerly named in the luminogenic organ of certain fishes or in the Pyrophorus noctilucus. Dubois mixed “cold” and culture plate during the exponential growth. This “hot” aqueous extracts of the insect lanterns and results from the accumulation of an auto-inducer discovered that a thermostable substrate (luciferin) in the medium, which induces the luciferase and a thermolabile component (luciferase) elicit a biosynthesis. flash of green light. Much later, McElroy (1947) It is believed that the acquisition of discovered that addition of ATP and Mg2+ ions is bioluminescence occurred discontinuously at least also necessary to enhance the in vitro and in vivo 30 times along the evolution, on the basis of the firefly bioluminescence. Success of the Dubois varied luciferase structures, enzymatic mechanisms experiment with any bioluminescent organism and luciferin nature clarified until now in distant also depends on molecular oxygen, a requirement luminous organisms. Kaskova et al. (2016) listed discovered by Robert Boyle (1668a, b) when nine luciferins identified up to the present: FMNH/ comparing the luminescence of decomposing long chain aldehyde in bacteria (Aliivibrio fisheri), fish (actually bacteria) and rotten wood (from linear tetrapyrrole in dinoflagellates (Lingulodinium saprophytic fungi) under ‘vaccum’ (sic) and air. He polyedra, formely Goniaulax), hispidin in fungi, also differed the nature of the flame of burning coal an aliphatic formylenol in a clam (Latia luciferin), (hot) from the shining wood (cold), both oxygen- two imidazopyrazines in crustaceans (Vargula, dependent phenomena. formerly Cypridina luciferin) and coelenterates Hundreds of marine fishes, jellyfishes, squids, (Renilla and Aequorea luciferin), a N-isovaleryl- mollusks, sea stars, crustaceans, annelids, in 3-aminopropanal in the earthworm Diplocardia, addition to bacteria and dinoflagellates, have been a peptide in another earthworm (Fridericia), and found to be luminescent, although the chemical a benzothiazolyl thiazole in coleopterans (Fig. 2). mechanisms of many of them had yet to be Luciferins of the blue-emitting fliesArachnocampa revealed. Terrestrial luminescent organisms are (New Zealand) and Orphelia (United States of less diversified, among them being beetles, flies, America) are still under investigation (Viviani et fungi, and millipedes. In general, bioluminescence al. 2002). serves intra- and interspecies communication Additionally, the reaction mechanisms of in mating, predation, camouflage, and grouping. bioluminescent systems follow distinct patterns Not obvious is the role of bioluminescence in of complexity. The bioluminescent system of the bacteria, dinoflagellates, fungi and other beings crustacean Vargula higendorfii (Cypridinidae) in lower branches of the evolutionary tree. is the simplest one. It requires only luciferin, Recently, comparative experiments with luminous luciferase, and oxygen for light emission, whereas mushrooms and green LED-illuminated artificial that of firefly lanterns also depends on ATP to acrylic ‘mushrooms’ were shown to equally attract activate the substrate (McElroy 1947, Wilson several classes of flying insects, which do not feed and Hastings 2013). In Renilla reniformis, the on
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