Skip to main content
Log in

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

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

(Fbr):

Fulgeochlizus bruchi

(Pang dGR):

Pyrophorus angustus dorsal green luciferase

(PangvYG):

Pyrophorus angustus ventral yellow-green luciferase

(Ppl_dGR):

Pyrophorus plagiophthalamus dorsal green luciferase

(Ppl_dYG):

Pyrophorus plagiophthalamus dorsal yellow-green luciferase

(Ppl_vYG):

Pyrophorus plagiophthalamus ventral yellow-green luciferase

(Ppl_vYE):

Pyrophorus plagiophthalamus ventral yellow luciferase

(Ppl_vOR):

Pyrophorus plagiophthalamus ventral orange luciferase

(Pme_dGR):

Pyrophorus mellifluus dorsal green luciferases

(Pme_vGR):

Pyrophorus mellifluus ventral green luciferases

(Pte):

Pyrearinus termitilluminans

(Ppy):

Photinus pyralis

(PxRE):

Phrixotrix hirtus red emitting luciferase

(Cdi):

Cratomorphus distinctus luciferase

References

  1. R. A. Crowson, A review of the classification of Cantharoidea (Coleoptera), with the definition of two new families, Cneoglossidae and Omethidae, Rev. Univ. Madrid, 1972, 21, 35–77.

    Google Scholar 

  2. J. F. Lawrence and A. F. Newton, in 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.

  3. W. D. McElroy and M. DeLuca, Chemistry of firefly bioluminescence, in Bioluminescence in Action, ed. P. Herring, Academic Press, New York, 1978, pp. 109–127.

    Google Scholar 

  4. K. V. Wood, The chemical mechanism and evolutionary development of beetle bioluminescence, Photochem. Photobiol., 1995, 62, 662–673.

    Article  CAS  Google Scholar 

  5. N. P. Colepicolo, C. Costa and E. J. H. Bechara, Brazilian species of elaterid luminescent beetles. Luciferin identification and bioluminescence spectra, Insect Biochem. Mol. Biol., 1986, 16, 803–810.

    Google Scholar 

  6. V. R. Viviani and E. J. H. Bechara, Biophysical and biochemical aspects of phengodid (railroadworms) bioluminescence, Photochem. Photobiol., 1993, 58, 615–622.

    Article  CAS  Google Scholar 

  7. K. V. Wood, in Bioluminescence and Chemiluminescence: Current Status, ed. P. Stanley and L. Kricka, John Wiley and Sons, Chichester, 1991, p, 543.

  8. 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 

  9. 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 

  10. V. R. Viviani, F. Arnoldi, A. J. Silva Neto, E. J. H. Bechara, T. L. Ohelmeyer and Y. Ohmiya, The structural origin and biological functions of pH-sensitivity in beetle luciferases, Photochem. Photobiol. Sci., 2008, 7, 159–169.

    Article  CAS  PubMed  Google Scholar 

  11. A. Roda, M. Guadigli, E. Michelini and M. Mirasoli, Bioluminescence in analytical chemistry and in vivo imaging, TrAC, Trends Anal. Chem., 2009, 28, 307–322.

    Article  CAS  Google Scholar 

  12. L. Mezzanotte, I. Que, E. Kaijzel, B. Branchini, A. Roda, C. Löwik, Sensitive dual color in vivo bioluminescence imaging using a new red codon optimized firefly luciferase and a green click-beetle luciferase, PLoS One, 2011, 6, 9.

    Article  CAS  Google Scholar 

  13. C. Costa, J. F. Lawrence, S. P. Rosa, Elateridae Leach, 1815, in Handbook of Zoology, Arthropoda, Insecta, Coleoptera, Beetles, Morphology and Systematics (Elateroidea, Bostridhiformia, Cucujiformia partim), Walter de Gruyter GmbH & Co.KG, Berlin, 2010, vol. 02, pp. 75–83.

    Google Scholar 

  14. C. Costa, Speciation and geographical patterns in Pyrophorus Bilberg, 1820 (Coleoptera, Elateridae, Pyrophorini), Pap. Avulsos Dep. Zool., Secr. Agric., Ind. Comer. (Sao Paulo), 1976, 29, 141–154.

    Google Scholar 

  15. J. N. L. Stibick, Classification of the Elateridae (Coleoptera). Relationships and classification of the subfamilies and tribes, Pacific Insects, 1979, 20, 145–186.

    Google Scholar 

  16. R. Sagegami-Oba, Y. Oba, H. Ôhira, Phylogenetic relationships of click beetles (Coleoptera: Elateridae) inferred from 28S ribossomal DNA: Insights into the evolution of bioluminescence in Elateridae, Mol. Phylogenet. Evol., 2007, 42, 410–421.

    Article  CAS  PubMed  Google Scholar 

  17. S. Stolz, K. V. Velez, M. Wood and J. L. Feder, Darwinian natural selection for orange bioluminescent color in a Jamaican click beetle, Proc. Natl. Acad. Sci. U. S. A., 2003, 100, 14955–14959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. S. Velez and J. L. Feder, Integrating biogeographic and genetic approaches to investigate the history of bioluminescent colour alleles in the Jamaican click beetle, Pyrophorus plagiophthalamus, Mol. Ecol., 2006, 15, 1393–1404.

    Article  CAS  PubMed  Google Scholar 

  19. J. L. Feder and S. Velez, Intergenic exchange, geographic isolation, and the evolution of bioluminescent color for Pyrophorus click beetles, Evolution, 2009, 5, 1203–1216.

    Article  Google Scholar 

  20. E. J. H. Bechara, Luminescent elaterid beetles: biochemical, biological and ecological aspects, Adv. Oxygenated Processes, 1989, 1, 123–178.

    Google Scholar 

  21. A. B. Lall, T. W. Cronin, A. A. Carvalho, J. M. Souza, M. P. Barros, C. V. Stevani, E. J. H. Bechara, D. F. Ventura, V. Viviani and A. A. Hill, Vision in click beetles (Coleoptera: Elateridae): pigments and spectral correspondence between visual sensitivity and species bioluminescence emission, J. Comp. Physiol., A, 2010, 196, 629–638.

    Article  Google Scholar 

  22. 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 

  23. C. Costa, Systematics and evolution of the tribes Pyrophorini and Heligmini, with description of Campyloxeninae, new subfamily (Col. Elat.), Arq. Zool., 1975, 26, 49–190.

    Article  Google Scholar 

  24. 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 

  25. 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 termitilluminans Luciferase, Photochem. Photobiol., 1999, 70, 254–260.

    Article  CAS  PubMed  Google Scholar 

  26. Y. Oba, M. Kumakazi and S. Inouye, Characterization of luciferases and its paralogue in the Panamanian luminous click-beetle Pyrophorus angustus: a click-beetle luciferase lacks the fatty acyl-CoA synthetic activity, Gene, 2010, 452, 1–6.

    Article  CAS  PubMed  Google Scholar 

  27. Y. Oba, K. Iida, M. Ojika and S. Inouye, Orthologous gene of beetle luciferase in non-luminous click beetle, Agrypnus binodulus (Elateridae), encodes a fatty acyl-CoA synthetase, Gene, 2008, 407, 169–175.

    Article  CAS  PubMed  Google Scholar 

  28. 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 

  29. A. J. Silva Neto, V. Scorsato, F. G. C. Arnoldi and V. R. Viviani, Pyrearinus termitilluminans larval click beetle luciferase: active site properties, structure and function relationships and comparison with other beetle luciferases, Photochem. Photobiol. Sci., 2009, 8, 1748–1754.

    Article  CAS  PubMed  Google Scholar 

  30. S. P. Rosa, C. Costa and N. Higashi, New data of the natural history and description of the immatures of Fulgeochlizus bruchi, a bioluminescent beetle from central brazil (Elateridae, Pyrophorini), Pap. Avulsos Dep. Zool., Secr. Agric., Ind. Comer. (Sao Paulo), 2010, 50, 635–641.

    Article  Google Scholar 

  31. J. D. Thompson, D. G. Higgins and T. J. Gibson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, 22, 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. A. J. Drummond and A. Rambaut, “BEAST: Bayesian evolutionary analysis by sampling trees”, BMC Evol. Biol., 2007, 7, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. A. Rambaut, FigTree: Tree Figure Drawing Tool Version 1.3.1, Institute of Evolutionary Biology, University of Edinburgh, 2007.

    Google Scholar 

  34. S. P. Rosa, Análise Filogenética e Revisão Taxonômica da Tribo Pyrophorini Candèze, 1863 (Coleoptera, Elateridae, Agrypinae), PhD thesis, University of São Paulo, 2007, p. 252.

    Google Scholar 

  35. F. C. Arnoldi, K. Ogoh, Y. Ohmiya and V. R. Viviani, Mitochondrial genome sequence of the Brazilian luminescent click beetle Pyrophorus divergens (Coleoptera: Elateridae): mitochondrial genes utility in the investigation of the evolutionary history of Coleoptera and its bioluminescence, Gene, 2007, 405, 1–9.

    Article  CAS  PubMed  Google Scholar 

  36. R. Kundrata and L. Bocak, The phylogeny and limits of Elateridae (Insecta, Coleoptera): is there a common tendency of click beetles to soft-bodiedness and neoteny?, Zoologica Scripta, 2011, 40, 364–378.

    Article  Google Scholar 

  37. F. G. C. Arnoldi, A. J. Silva-Neto and V. Viviani, Molecular insights on the evolution of the lateral and head lantern luciferases and bioluminescence colors in Mastinocerini railroad-worms (Coleoptera: Phengodidae), Photochem. Photobiol. Sci., 2010, 9, 87–92.

    Article  CAS  PubMed  Google Scholar 

  38. V. R. Viviani, F. G. Arnoldi, M. Brochetto-Braga and Y. Ohmiya, Cloning and characterization of the cDNA for the Brazilian Cratomorphus 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 

  39. J. C. Day, T. I. Goodall and M. J. Bailey, The evolution of the adenylate-forming protein family in beetles: multiple luciferase gene paralogues in fireflies and glow-worms, Mol. Phylogenet. Evol., 2009, 50, 93–101.

    Article  CAS  PubMed  Google Scholar 

  40. Y. Oba, N. Mori, M. Yoshida and S. Inouye, Identification and characterization of a luciferase isotype in the Japanese firefly, Luciola cruciata, involving in the dim glow of firefly eggs, Biochemistry, 2010, 49, 10788–10795.

    Article  CAS  PubMed  Google Scholar 

  41. 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 

  42. 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 

  43. G. D. Kutuzova, R. R. Hannah and K. V. Wood, Bioluminescence color variation and kinetic behavior relationships among luciferases, Biolum. Chemilumin., 1996, 248–252.

    Google Scholar 

  44. K. V. Wood, Luc gene: introduction of color into biolumenscence assays, J. Biolumin. Chemilumin., 1990, 5, 107–114.

    Article  CAS  PubMed  Google Scholar 

  45. 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 

  46. V. R. Viviani, D. Amaral, R. Prado and F. G. C. Arnoldi, A new blue-shifted luciferase from the Brazilian Amydetes fanestratus (Coleoptera: Lampyridae) firefly: molecular evolution and structural/functional properties, Photochem. Photobiol. Sci., 2011, 10, 1879–1886.

    Article  CAS  PubMed  Google Scholar 

  47. 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 

  48. V. R. Viviani, T. L. Oehlmeyer, F. G. C. Arnoldi, 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 

  49. S. Hosseinkhani, Molecular enigma of multicolor bioluminescence of firefly luciferase, Cell. Mol. Life Sci., 2011, 68, 1167–1182.

    Article  CAS  PubMed  Google Scholar 

  50. N. K. H. Tafreshi, S. Hosseinkhani, M. Sadeghizadeh, M. Sadeghi, B. Ranjbar, H. Naderi-Manesh, The influence of insertion of a critical residue (Arg356) in structure and bioluminescence spectra of firefly luciferase, J. Biol. Chem., 2007, 282, 8641–8647.

    Article  CAS  PubMed  Google Scholar 

  51. A. Moradi, S. Hosseinkhani, H. Naderi-Manesh, M. Sadeghizadeh and B. A. Alipour, Effect of charge distribution in a flexible loop on the bioluminescence color of fireflies luciferase, Biochemistry, 2009, 48, 575–582.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vadim R. Viviani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amaral, D.T., Prado, R.A. & Viviani, V.R. 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. Photochem Photobiol Sci 11, 1259–1267 (2012). https://doi.org/10.1039/c2pp25037c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c2pp25037c

Navigation