Skip to main content
Log in

An ancestral luciferase in the Malpighi tubules of a non-bioluminescent beetle!

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

Abstract

The evolutionary origin of beetle bioluminescence is enigmatic. Previously, weak luciferase activity was found in the non-bioluminescent larvae of Tenebrio molitor (Coleoptera: Tenebrionidae), but the detailed tissular origin and identity of the luciferase-like enzyme remained unknown. Using a closely related giant mealworm, Zophobas morio, here we show that the luciferase-like enzyme is located in the Malpighi tubules. cDNA cloning of this luciferase like enzyme, showed that it is a short AMP-ligase with weak luciferase activity which diverged long ago from beetle luciferases. The results indicate that the potential for bioluminescence in AMP-ligases is very ancient and provide a first reasonable protoluciferase model to investigate the origin and evolution of beetle luciferases.

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

References

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

    Article  CAS  Google Scholar 

  2. V. R. Viviani, The Origin, Diversity and Structure Function Relationships of Insects Luciferases Cell. Mol. Life Sci 2002 59 1833–1850.

    Article  CAS  Google Scholar 

  3. J. W. Hastings, Biological diversity, chemical mechanisms and evolutionary origins of bioluminescent systems J. Molecular Evolution 1983 19 309–321.

    Article  CAS  Google Scholar 

  4. J. F. Rees, B. De Wergifosse, O. Noiset, M. Debuisson, B. Janssens, M. E. Thompson, J. Exp. Biol 1998 201 1211.

    Article  CAS  Google Scholar 

  5. V. R. Viviani and J. H. Bechara, Larval Tenebrio molitor (Coleoptera: Tenebrionidae) fat body extracts catalyze d-luciferin and ATP-dependent chemiluminescence. A luciferase-like enzyme Photochem. Photobiol. 1996 63 713–718.

    Article  CAS  Google Scholar 

  6. Y. Oba, M. Sato and S. Inouye, Cloning and characterization of the homologous genes of firefly luciferase in the mealworm beetle, Tenebrio molitor Insect Mol. Biol. 2006 15 293–299.

    Article  CAS  Google Scholar 

  7. V. R. Viviani and Y. Ohmiya, Bovine serum albumin displays luciferase-like activity in presence of luciferyl-adenylate: insights on the origin of protoluciferase activity and bioluminescence colors Luminescence 2006 21 262–267.

    Article  CAS  Google Scholar 

  8. E. Conti, N. P. Franks and P. Brick, Crystal Structure of Firefly Luciferase Throws Light on a Super Family of Adenylate-forming Enzymes Structure 1996 4 287–298.

    Article  CAS  Google Scholar 

  9. 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  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. 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 

  13. V. R. Viviani, F. M. Okawachi, V. Scorsato and F. C. Abdalla, CCD imaging of basal bioluminescence in larval fireflies: clues on the anatomic origin and evolution of bioluminescence Photochem. Photobiol. Sci. 2008 7 448–452.

    Article  CAS  Google Scholar 

  14. K. M. Knights and C. J. Drogemuller, Xenobiotic-CoA ligases: kinetic and molecular characterization Current Drug Metab. 2000 1 49–66.

    Article  CAS  Google Scholar 

  15. W. C. Dauterman, in Comprehensive Insect Physiology, Biochemistry and Pharmacology, ed. G. A. Kerkut and L. I. Gilbert, Pergamon Press, New York, 1985, 18, pp. 713–730.

    Google Scholar 

  16. J. B. Gattenby, The Australasian mycetophilid glow-worms. Trans. R. Soc. N. Z. 1960 88 577–593.

    Google Scholar 

  17. D. L. Swofford, PAUP. Phylogenetic, Analysis Using Parsimony (and Other Methods), Version 4, Sinauer Associates, Sunderland, Massachusetts, 1998.

    Google Scholar 

  18. N. Saitou and M. Nei, The neighbor-joining method: a new method for reconstruction of phylogenetic trees. Mol. Biol. Evol. 1987 4 406–425.

    CAS  PubMed  Google Scholar 

  19. V. Makarenkov, T-Rex: reconstructing and visualizing phylogenetic trees and reticulation networks Bioinformatics 2001 17 664–668.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. R. Viviani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Viviani, V.R., Prado, R.A., Arnoldi, F.C.G. et al. An ancestral luciferase in the Malpighi tubules of a non-bioluminescent beetle!. Photochem Photobiol Sci 8, 57–61 (2009). https://doi.org/10.1039/b817114a

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b817114a

Navigation