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A new blue-shifted luciferase from the Brazilian Amydetes fanestratus (Coleoptera: Lampyridae) firefly: molecular evolution and structural/functional properties

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Abstract

Firefly luciferases usually produce bioluminescence in the yellow-green region, with colors in the green and yellow-orange extremes of the spectrum being less common. Several firefly luciferases have already been cloned and sequenced, and site-directed mutagenesis studies have already identified important regions and residues for bioluminescence colors. However the structural determinants and mechanisms of bioluminescence colors turned out to be elusive, mainly when comparing luciferases with a high degree of divergence. Thus comparison of more similar luciferases producing colors in the two extremes of the spectrum could be revealing. The South-American fauna of fireflies remains largely unstudied, with some unique taxa that are not found anywhere else in the world and that produce a wide range of bioluminescence colors. Among them, fireflies of the genus Amydetes are especially interesting because its taxonomical status as an independent subfamily or as a tribe is not yet solved, and because they usually produce a continuous bright blue-shifted bioluminescence. In this work we cloned the cDNA for the luciferase of the Atlantic rain forest Amydetes fanestratus firefly, which is found near Sorocaba municipality (São Paulo, Brazil). Despite showing a higher degree of identity with the South-American Cratomorphus, the European Lampyris and the Asiatic Pyrocoelia, phylogenetical analysis of the luciferase sequence support the inclusion of Amydetes as an independent subfamily. Amydetes luciferase displays one of the most blue-shifted emission spectra (λmax = 538 nm) among beetle luciferases, with lower pH-sensitivity and higher affinity for ATP when compared to other luciferases, making this luciferase attractive for sensitive ATP and reporter assays.

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References

  1. V. R. Viviani, The origin, diversity and structure function relationships of insect luciferases, Cell. Mol. Life Sci., 2002, 59, 1833–1850.

    Article  CAS  PubMed  Google Scholar 

  2. A. B. Lall, H. H. Seliger, W. H. Biggley and J. E. Lloyd, Ecology of colors of firefly bioluminescence, Science, 1980, 210, 560–562.

    Article  CAS  PubMed  Google Scholar 

  3. H. H. Seliger and W. D. McElroy, The colors of firefly bioluminescence: enzyme configuration and species specificity, Proc. Natl. Acad. Sci. U.S.A., 1964, 52, 75–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. W. H. Biggley, J. E. Lloyd and H. H. Seliger, The spectral distribution of firefly light II, J. Gen. Physiol., 1967, 50, 1681–1692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. V. R. Viviani and E. J. H. Bechara, Bioluminescence of Brazilian fireflies (Coleoptera: Lampyridae): spectral distribution and pH effect on luciferase-elicited colors. Comparison with elaterid and phengodid luciferases, Photochem. Photobiol., 1995, 62, 490–495.

    Article  CAS  Google Scholar 

  6. V. R. Viviani, Fireflies (Coleoptera: Lampyridae) from southeastern Brazil habitats, life history and bioluminescence, Ann. Entomol. Soc. Am., 2001, 94, 129–145.

    Article  Google Scholar 

  7. J. R. de Wet, K. V. Wood, D. R. Helinsky and M. DeLuca, Cloning of firefly luciferase cDNA and expression of active luciferase in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A., 1985, 82, 7870–7873.

    Article  PubMed  PubMed Central  Google Scholar 

  8. H. Tatsumi, T. Masuda, N. Kajiyama and E. Nakano, Luciferase cDNA from Japanese firefly, Luciola cruciata: Cloning, structure and expression in Escherichia coli, Luminescence, 1989, 3, 75–78.

    CAS  Google Scholar 

  9. J. H. Devine, G. D. Kutuzova, V. A. Green, N. N. Ugarova and T. O. Baldwin, Luciferase from the east European firefly Luciola mingrelica: cloning and nucleotide of cDNA, overexpression in Escherichia coli and purification of the enzyme, Biochem. Biophys. Acta, Bio, 1993, 1173, 121–132.

    CAS  Google Scholar 

  10. Y. Ohmiya, N. Ohba, H. Toh and F. Tsuji, Cloning, expression, and sequence analysis of cDNA for the luciferases from the Japanese fireflies Pyrocoelia miyako and Hotaria parvula, Photochem. Photobiol., 1995, 62, 309–313.

    Article  CAS  PubMed  Google Scholar 

  11. G. B. Sala-Newby, C. M. Thomson and A. K. Campbell, Sequence and biochemical similarities between the luciferases of the glow-worm Lampyris noctiluca and the firefly Photinus pyralis, Biochem. J., 1996, 313, 761–767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. K. W. Wood, Y. A. Lam, H. H. Seliger and W. D. McElroy, Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors, Science, 1989, 244, 700–702.

    Article  CAS  PubMed  Google Scholar 

  13. L. Ye, L. M. Buck, H. J. Scaeffer and F. R. Leach, Cloning and sequencing of a cDNA for firefly luciferase from Photuris pennsylvanica, Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol., 1997, 1339, 39–52.

    Article  CAS  Google Scholar 

  14. V. R. Viviani, A. C. R. Silva, G. L. O. Perez, R. V. Santelli, E. J. H. Bechara and F. C. Reinach, Cloning and molecular characterization of the cDNA for the Brazilian larval click-beetle Pyrearinus termitillumi-nans luciferase, Photochem. Photobiol., 1999, 70, 254–260.

    Article  CAS  PubMed  Google Scholar 

  15. V. R. Viviani, E. J. H. Bechara and Y. Ohmiya, Cloning, sequence analysis, and expression of active Phrixothrix railroad-worms luciferases: relationship between bioluminescence spectra and primary structures, Biochemistry, 1999, 38, 8271–8279.

    Article  CAS  PubMed  Google Scholar 

  16. Y. Ohmiya, M. Sumiya, V. R. Viviani and N. Ohba, Comparative aspects of a luciferase molecule from the Japanese luminous beetle, Ragophthalmus ohbai, Sci. Rept. Yokosuka City Mus., 2000, 47, 31–38.

    Google Scholar 

  17. B. S. Alipour, S. Hosseinkhani, M. Nikkhah, H. Naderi-Manesh, M. J. Chaichi and S. K. Osallo, Molecular cloning, sequence analysis, and expression of a cDNA encoding the luciferase from the glow-worm, Lampyris turkestanicus, Biochem. Biophys. Res. Commun., 2004, 325, 215–222.

    Article  PubMed  CAS  Google Scholar 

  18. V. R. Viviani, F. G. Arnoldi, M. Brochetto-Braga and Y. Ohmiya, Cloning and characterization of the cDNA for the Brazilian Crato-morphus distinctus larval firefly luciferase: similarities with European Lampyris noctiluca and Asiatic Pyrocoelia luciferases, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2004, 139, 151–156.

    Article  CAS  Google Scholar 

  19. V. R. Viviani, T. L. Oehlmeyer, F. G. Arnoldi and M. R. Brochetto-Braga, A new firefly luciferase with bimodal spectrum: identification of structural determinants of spectral pH-sensitivity in firefly luciferases, Photochem. Photobiol., 2005, 81, 843–848.

    Article  CAS  PubMed  Google Scholar 

  20. E. Conti, N. P. Franks and P. Brick, Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes, Structure, 1996, 4, 287–298.

    Article  CAS  PubMed  Google Scholar 

  21. T. Nakatsu, S. Ichiyama, J. Hiratake, A. Saldanha, N. Kobashi, K. Sakata and H. Kato, Structural basis for the spectral difference in luciferase bioluminescence, Nature, 2006, 440, 372–376.

    Article  CAS  PubMed  Google Scholar 

  22. B. R. Branchini, R. A. Magyar, M. H. Murtiashaw, S. M. Anderson and M. Zimmer, Site-directed mutagenesis of Histidine 245 in firefly luciferase: a proposed model of the active site, Biochemistry, 1998, 37, 15311–15319.

    Article  CAS  PubMed  Google Scholar 

  23. B. R. Branchini, R. A. Magyar, M. H. Murtiashaw and N. C. Portier, The role of active site residue arginine 218 in firefly luciferase bioluminescence, Biochemistry, 2001, 40, 2410–2418.

    Article  CAS  PubMed  Google Scholar 

  24. B. R. Branchini, T. L. Southworth, M. H. Murtiashaw, H. Boije and S. E. Fleet, A mutagenesis study of the putative luciferin binding site residues of firefly luciferase, Biochemistry, 2003, 42, 10429–10436.

    Article  CAS  PubMed  Google Scholar 

  25. N. Kajiyama and E. Nakano, Isolation and characterization of mutants of firefly luciferase which produce different colors of light, Protein Eng., Des. Sel., 1991, 4, 691–693.

    Article  CAS  Google Scholar 

  26. S. V. Mamaev, A. L. Laikhter, T. Arslanand and S. M. Hecht, Firefly luciferase: Alteration of the color of emitted light resulting from substitutions at position 286a, J. Am. Chem. Soc., 1996, 118, 7243–7244.

    Article  CAS  Google Scholar 

  27. H. Ueda, H. Yamanouchi, A. Kitayama, K. Inoue, T. Hirano, E. Suzuki, T. Nagamune, and Y. Ohmiya, His-433 as a key residue for the color difference in firefly luciferase Hotaria parvula, in Bioluminescence and Chemiluminescence: Molecular Reporting with Photons, ed. J. W. Hastings, L. J. Kricka and P. E. Stanley, J. Wiley and Sons, Chichester, 1996, pp. 216–219.

    Google Scholar 

  28. A. Kitayama, H. Yoshizaki, Y. Ohmiya, H. Ueda and T. Naga-mune, Creation of a thermostable firefly luciferase with pH-insensitive luminescent color, Photochem. Photobiol., 2003, 77, 333–338.

    Article  CAS  PubMed  Google Scholar 

  29. N. N. Ugarova, L. G. Maloshenok, I. V. Uporov and M. I. Koksharov, Bioluminescence spectra of native and mutant firefly luciferases as a function of pH, Biochemistry, 2005, 70, 1262–1267.

    CAS  PubMed  Google Scholar 

  30. V. R. Viviani, A. J. Silva Neto, F. G. C. Arnoldi, J. A R. G. Barbosa and Y. Ohmiya, The influence of the loop between residues 223-235 in beetle luciferase bioluminescence spectra: a solvent gate for the active site of pH-sensitive luciferases, Photochem. Photobiol., 2007, 83, 1–7.

    Article  Google Scholar 

  31. V. R. Viviani, F. G. C. Arnoldi, A. J. S. Neto, T. L. Oehlmeyer, E. J. H. Bechara and Y. Ohmiya, The structural origin and biological function of pH-sensitivity in firefly luciferases, Photochem. Photobiol. Sci., 2008, 7, 159–169.

    Article  CAS  PubMed  Google Scholar 

  32. G. D. Kutuzova, R. R. Hanna, and K. W. Wood, Bioluminescence color variation and kinetic behavior relationship among beetle luciferases, in Bioluminescence and Chemiluminescence: reporting with photons, ed. J. W. Hastings, L. J. Kricka and P. Stanley, J. Wiley and Sons, Chichester, 1996, pp 248.

    Google Scholar 

  33. F. A. McDermott, The taxonomy of the Lampyridae (Coleoptera), Trans. Am. Entomol. Soc., 1964, 90, 1–72.

    Google Scholar 

  34. J. F. Lawrence, and A. F. Newton, Families and subfamilies of Coleoptera (with selected genera, notes, references and data on family-group names), in Biology, phylogeny and classification of Coleoptera, ed. J. Pakaluk and S. A. Slipinsky, Muzeum i Instytut Zoologii PAN, Warsaw, Poland, 1995, pp. 779–1006.

    Google Scholar 

  35. V. R. Viviani, M. Y. Rocha and O. Hagen, Fauna de besouros bioluminescentes (Coleoptera: Elateroidea: Lampyridae; Phengodidae, Elateridae) nos munićıpios de Campinas, Sorocaba-Votornatim e Rio Claro-Limeira (SP, Brasil): biodiversidade influencia da urbanização, Biota Neotropica, 2010, 10, 103–116.

    Article  Google Scholar 

  36. M. A. Larkin, G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson and D. G. Higgins, Clustal W and Clustal X version 2.0, Bioinformatics, 2007, 23(21), 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  37. A. Sali and T. L. Blundell, Comparative protein modeling by satisfaction of spatial restraints, J. Mol. Biol., 1993, 234, 779–815.

    Article  CAS  PubMed  Google Scholar 

  38. W. L. Delano, The PyMol molecular graphics system, 2002, available at: http://www.pymol.org. matrix choice, Nucleic Acids Res., 1994, 22, 4673–4680.

    Article  Google Scholar 

  39. D. L. Swofford, PAUP*, Phylogenetic analysis using parsimony (*and other methods), Version 4, Sinauer Associates, Sunderland, Massachusetts, available at http://paup.csit.fsu.edu/Cmd_ref_v2.pdf.

  40. N. Saitou and M. Nei, The neighbor-joining method: a new method for reconstruction of phylogenetic trees, Mol. Biol. Evol., 1987, 4, 406–25.

    CAS  PubMed  Google Scholar 

  41. T. Hirano, Y. Hasumi, K. Ohtsuka, S. Maki, H. Niwa and D. Hashizume, Spectroscopic studies of the light-color modulation mechanism of firefly (beetle) bioluminescence, J. Am. Chem. Soc., 2009, 131, 2385.

    Article  CAS  PubMed  Google Scholar 

  42. B. R. Branchini, D. M. Ablamsky, M. H Murtishaw, L. Uzasci, H. Fraga and T. Southworth, Thermostable red and green emitting light-producing firefly luciferase mutants for bioluminescence reporter applications, Anal. Biochem., 2007, 361, 253–262.

    Article  CAS  PubMed  Google Scholar 

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Viviani, V.R., Amaral, D., Prado, R. et al. A new blue-shifted luciferase from the Brazilian Amydetes fanestratus (Coleoptera: Lampyridae) firefly: molecular evolution and structural/functional properties. Photochem Photobiol Sci 10, 1879–1886 (2011). https://doi.org/10.1039/c1pp05210a

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