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Luciferase from Fulgeochlizus Bruchi (Coleoptera: Elateridae), a Brazilian

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Luciferase from Fulgeochlizus Bruchi (Coleoptera: Elateridae), a Brazilian Photochemical & Dynamic Article Links Photobiological Sciences Cite this: Photochem. Photobiol. Sci., 2012, 11, 1259 www.rsc.org/pps PAPER Luciferase from Fulgeochlizus bruchi (Coleoptera:Elateridae), a Brazilian click-beetle with a single abdominal lantern: molecular evolution, biological function and comparison with other click-beetle luciferases Danilo T. Amaral,a,b Rogilene A. Pradoa,b and Vadim R. Viviani*a,b Received 16th February 2012, Accepted 21st March 2012 DOI: 10.1039/c2pp25037c Bioluminescent click-beetles emit a wide range of bioluminescence colors (λMax = 534–594 nm) from thoracic and abdominal lanterns, which are used for courtship. Only the luciferases from Pyrophorus and Pyrearinus species were cloned and sequenced. The Brazilian Fulgeochlizus bruchi click-beetle, which inhabits the Central-west Cerrado (Savannas), is noteworthy because, differently from other click-beetles, the adult stage displays only a functional abdominal lantern, which produces a bright green bioluminescence for sexual attraction purposes, and lacks functional thoracic lanterns. We cloned the cDNA for the abdominal lantern luciferase of this species. Notably, the primary sequence of this luciferase showed slightly higher identity with the green emitting dorsal lantern luciferases of the Pyrophorus genus instead of the abdominal lanterns luciferases. This luciferase displays a blue-shifted spectrum (λMax = 540 nm), which is pH-insensitive from pH 7.5 to 9.5 and undergoes a slight red shift and broadening above this pH; the lowest KM for luciferin among studied click-beetle luciferases, and the highest optimum pH (9.0) ever reported for a beetle luciferase. At pH 9.0, the KM for luciferin increases, showing a decrease of affinity for this substrate, despite the higher activity. The slow luminescence decay rate of F. bruchi luciferase in vitro reaction could be an adaptation of this luciferase for the long and sustained in vivo luminescence display of the click-beetle during the courtship, and could be useful for in vivo intracellular imaging. – Introduction compactness.7 10 Beetle luciferases emitting different biolumi- nescence colors have acquired a wide range of applications Bioluminescent beetles are found mainly in the Elateroidea as bioanalytical reagents, reporter genes for biosensors and superfamily, within Lampyridae (fireflies), Phengodidae (rail- bioimaging.11,12 1,2 roadworms) and Elateridae (click-beetles). Depending on the Among bioluminescent beetles, Elateridae is the richest family lantern and life stage, they emit different bioluminescence with about 9000 described species in the world,13 however, only colors, ranging from green to red, as ecological adaptations to a small number of them (about 200 species), occurring in the different photic environments and biological functions. Different Agrypinae subfamily2,13–16 within the Pyrophorini and Campy- bioluminescence colors are determined by luciferase structure loxenini tribes, are luminescent. In the adult stage, biolumines- differences, since the luciferin–luciferase reaction, which cent click-beetles usually have two sets of lanterns, which are involves an ATP-dependent oxidation of D-luciferin, leading to used for different purposes:17–19 two thoracic lanterns, which 3,4 excited oxyluciferin, is essentially identical, involving the emit green to yellow bioluminescence and are believed to be 5,6 same substrates and homologous luciferases. Mechanistic, used for defensive and sexual attraction purposes,20,21 and an structural and functional studies suggest that beetle luciferase abdominal lantern emitting green to orange bioluminescence, active sites may determine bioluminescence colors through which is activated during flight for sexual communication pur- non-specific (polarity) and specific interactions (base) with poses.5,20,22 However, the specific biological roles of these lan- the emitter (excited oxyluciferin), as well as conformational terns and their colors are still under scrutiny. In the larval stage, changes affecting specific and non-specific interactions and click-beetles usually emit green bioluminescence from prothor- acic lanterns and from several small spots spread along the 23 aLaboratory of Biochemistry and Biotechnology of Bioluminescence, body. Most studied click-beetles species do not show geo- Graduate Program of Biotechnology and Environmental Monitoring, graphical variation of the bioluminescence color in each Department of Physics, Chemistry and Mathematics, Federal University lantern,20 however, the Jamaican P. plagiophthalamus displays of São Carlos (UFSCar), Campus of Sorocaba, Sorocaba, SP, Brazil. an intriguing geographical variation of bioluminescence colors, E-mail: [email protected] bDepartment of Evolutive Genetics and Molecular Biology, Federal mainly in the abdominal lanterns, indicating an ongoing natural University of São Carlos (UFSCar), São Carlos, SP, Brazil selection process. The orange color found in the abdominal This journal is © The Royal Society of Chemistry and Owner Societies 2012 Photochem. Photobiol. Sci., 2012, 11, 1259–1267 | 1259 lanterns of some individuals may have recently evolved as an green to yellow-orange.5,21 The Brazilian click-beetle Fulgeosh- adaptation of bioluminescence against nocturnal predators, lizus bruchi, which is found in the Central-west Cerrado (Savan- which are visually poorly sensitive to red shifted colors, to nas), is unique because it displays only a functional abdominal decrease spectral competition with other bioluminescent beetles, lantern, which emits green light, and is lacking functional thor- which usually emit in the green-yellow range, or for sexual acic lanterns. During the spring evenings, adult males fly emit- selection.17,18 This wide variety of bioluminescent colors ting an intense greenish light from the abdominal lantern, must have been originated by strong effects of geographic iso- whereas females in the grass answer with their abdominal lan- lation, probably vicariance events, combined with intergenic terns.30 Here we report the cloning, sequence analysis and exchange.19 characterization of the luciferase cDNA from the abdominal The luciferases from a few click-beetle species, mostly for the lantern of this click-beetle and the expression and characteriz- Pyrophorus genus, were cloned and sequenced: the green, ation of the recombinant enzyme. yellow-green, yellow and orange emitting isozymes from the 24 Jamaican click-beetle Pyrophorus plagiophthalamus, the luci- Material and methods ferase from the Brazilian larval click-beetle Pyrearinus termitil- 25 luminans, which elicits the phenomenon of luminous termite Insects mounds in Central-West Brazil and displays the most blue- shifted bioluminescence spectrum among cloned beetle luci- Adults of F. bruchi (Fig. 1) were attracted to chemiluminescent ferases, and the luciferases from the ventral and dorsal lantern of light sticks (green light) and manually collected during late eve- the Central American Pyrophorus mellifluous17 and Pyrophorus nings of November of 2009 at Fazenda Sta. Cruz in the proxi- angustus.26 A luciferase-like enzyme from the Japanese Agrypi- mity of the Parque Nacional das Emas (Costa Rica-MS, Brazil). fi nus binodulus,27 but which does not emit light, was also cloned. The specimens were identi ed by Vadim Viviani (UFSCAR) by − Click-beetle luciferases were functionally classified as pH-insen- comparison with a personal collection and frozen at 80 °C. sitive because their luminescence spectra do not shift at acidic 28 pH, higher temperatures and in the presence of heavy metals, cDNA cloning however, it has been shown that at pH above 10.0, the emission spectra undergoes a red shift and broadening.29 Only the lucifer- cDNA cloning was performed using the SuperScript plasmid ase of P. plagiophtalamus and P. termitilluminans have been system with Gateway technology (Invitrogen). The total RNA characterized in more detail.24,29 Chimerization and site-directed from lanterns was isolated with Trizol reagent and mRNA was 25 mutagenesis studies with these enzymes have already shown purified using oligo-dT resin according to Viviani et al. The some important regions in click-beetle luciferases structures first and second cDNA strands were synthesized with the Super- responsible for bioluminescence colors: the region between resi- script/Gateway kit, Sal I adapters were ligated to the cDNA and dues 220–2477 which later was shown to contain the luciferin the cDNA cloned into the pSPORT-1 plasmid. The ligation reac- binding site motif 242HHGF245,28 the important luciferin tion was used to transform ultra-competent XL1-Blue cells from binding site shielding loop between residues 223–2359 and the STRATAGENE. The transformed colonies were plated on LB/ loop between residues 350–365. However, the structural determi- Amp plates containing 1 mM IPTG and grown overnight at nants and the mechanisms of bioluminescence color determi- 37 °C, followed by a period of protein expression induction at nation are not yet fully understood.10 22 °C during 12 h. The plates were then sprayed with 1 mM Brazil has the largest number of luminescent click-beetles in D-luciferin and exposed to an ATTO model LightCapture II CCD the world, occurring in different genera: Pyrophorus, Pyreari- camera system (Tokyo, Japan), for imaging bioluminescent posi- nus, Hapsodrilus, Hypsiophtalmus, Agnostelater, Coctilelater, tive clones. The positive colonies were isolated and submitted to Compsoplinthus, Deilelater, Hifo, Ignelater, Lygelater, Mero- three other
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