, Volume 24, Issue 4, pp 679–686 | Cite as

Evidence for evolutionary constraints in Drosophila metal biology

  • Maryam Sadraie
  • Fanis Missirlis


Mutations in single Drosophila melanogaster genes can alter total body metal accumulation. We therefore asked whether evolutionary constraints maintain biologically abundant metal ions (iron, copper, manganese and zinc) to similar concentrations in different species of Drosophilidae, or whether metal homeostasis is a highly adaptable trait as shown previously for triglyceride and glycogen storage. To avoid dietary influences, only species able to grow and reproduce on a standard laboratory medium were selected for analysis. Flame atomic absorption spectrometry was used to determine metal content in 5-days-old adult flies. Overall, the data suggest that the metallome of the nine species tested is well conserved. Meaningful average values for the Drosophilidae family are presented. Few statistically significant differences were noted for copper, manganese and zinc between species. In contrast, Drosophila erecta and Drosophila virilis showed a 50% increase above average and a 30% decrease below average in iron concentrations, respectively. The changes in total body iron content correlated with altered iron storage in intestinal ferritin stores of these species. Hence, the variability in iron content could be accounted for by a corresponding adaptation in iron storage regulation. We suggest that the relative expression of the multitude of metalloenzymes and other metal-binding proteins remains overall similar between species and likely determines relative metal abundances in the organism. The availability of a complete and annotated genome sequence of different Drosophila species presents opportunities to study the evolution of metal homeostasis in closely related organisms that have evolved separately for millions or dozens of million years.


Transition metals Insect physiology Ferritin iron stores Metallomics 



We thank Ms. Joanna Szular for assistance with the metal measurements, Rudi Costa for sending us wild type D. melanogaster strains, Brenda Thake for constructive discussions and Christoph Metzendorf for critical comments on the draft manuscript. Special thanks to the San Diego Drosophila Species Stock Center for making available the fly species and providing training to Maryam Sadraie in the 2009 Drosophila species identification workshop. This work was partially supported by a European Commission Marie Curie Re-Integration Grant “DrosoFela” (MIRG-CT-2007-204832) to Fanis Missirlis.


  1. Balamurugan K, Egli D, Hua H, Rajaram R, Seisenbacher G, Georgiev O, Schaffner W (2007) Copper homeostasis in Drosophila by complex interplay of import, storage and behavioral avoidance. EMBO J 26(4):1035–1044PubMedCrossRefGoogle Scholar
  2. Bettedi L, Aslam MF, Mandilaras K, Szular J, Missirlis F (2011) Lack of a multicopper oxidase reverts iron depletion in intestines of Malvolio mutant flies. J Exp Biol (in press)Google Scholar
  3. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450(7167):203–218PubMedCrossRefGoogle Scholar
  4. Gutierrez L, Sabaratnam N, Aktar R, Bettedi L, Mandilaras K, Missirlis F (2010) Zinc accumulation in heterozygous mutants of fumble, the pantothenate kinase homologue of Drosophila. FEBS Lett 584(13):2942–2946PubMedCrossRefGoogle Scholar
  5. Lind MI, Missirlis F, Melefors O, Uhrigshardt H, Kirby K, Phillips JP, Soderhall K, Rouault TA (2006) Of two cytosolic aconitases expressed in Drosophila, only one functions as an iron-regulatory protein. J Biol Chem 281(27):18707–18714PubMedCrossRefGoogle Scholar
  6. Lonnerdal B, Kelleher SL (2009) Micronutrient transfer: infant absorption. Adv Exp Med Biol 639:29–40PubMedCrossRefGoogle Scholar
  7. Markow TA, O’Grady PM (2007) Drosophila biology in the genomic age. Genetics 177(3):1269–1276PubMedCrossRefGoogle Scholar
  8. Matzkin LM, Markow TA (2009) Transcriptional regulation of metabolism associated with the increased desiccation resistance of the cactophilic Drosophila mojavensis. Genetics 182(4):1279–1288PubMedCrossRefGoogle Scholar
  9. McNulty M, Puljung M, Jefford G, Dubreuil RR (2001) Evidence that a copper-metallothionein complex is responsible for fluorescence in acid-secreting cells of the Drosophila stomach. Cell Tissue Res 304(3):383–389PubMedCrossRefGoogle Scholar
  10. Mehta A, Deshpande A, Missirlis F (2008) Genetic screening for novel Drosophila mutants with discrepancies in iron metabolism. Biochem Soc Trans 36(Pt 6):1313–1316PubMedCrossRefGoogle Scholar
  11. Mehta A, Deshpande A, Bettedi L, Missirlis F (2009) Ferritin accumulation under iron scarcity in Drosophila iron cells. Biochimie 91(10):1331–1334PubMedCrossRefGoogle Scholar
  12. Metzendorf C, Lind MI (2010) Drosophila mitoferrin is essential for male fertility: evidence for a role of mitochondrial iron metabolism during spermatogenesis. BMC Dev Biol 10:68PubMedCrossRefGoogle Scholar
  13. Metzendorf C, Wu W, Lind MI (2009) Overexpression of Drosophila mitoferrin in l(2)mbn cells results in dysregulation of Fer1HCH expression. Biochem J 421(3):463–471PubMedCrossRefGoogle Scholar
  14. Missirlis F, Kosmidis S, Brody T, Mavrakis M, Holmberg S, Odenwald WF, Skoulakis EM, Rouault TA (2007) Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 177(1):89–100PubMedCrossRefGoogle Scholar
  15. Odenwald WF, Rasband W, Kuzin A, Brody T (2005) EVOPRINTER, a multigenomic comparative tool for rapid identification of functionally important DNA. Proc Natl Acad Sci USA 102(41):14700–14705PubMedCrossRefGoogle Scholar
  16. Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5(5):333–340PubMedCrossRefGoogle Scholar
  17. Pitnick S, Markow TA, Spicer GS (1995) Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci USA 92(23):10614–10618PubMedCrossRefGoogle Scholar
  18. Poulson DF, Bowen VT (1952) Organization and function of the inorganic constituents of nuclei. Exp Cell Res Suppl 2:161–180Google Scholar
  19. Selvaraj A, Balamurugan K, Yepiskoposyan H, Zhou H, Egli D, Georgiev O, Thiele DJ, Schaffner W (2005) Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev 19(8):891–896PubMedCrossRefGoogle Scholar
  20. Sharp P, Srai SK (2007) Molecular mechanisms involved in intestinal iron absorption. World J Gastroenterol 13(35):4716–4724PubMedGoogle Scholar
  21. Southon A, Farlow A, Norgate M, Burke R, Camakaris J (2008) Malvolio is a copper transporter in Drosophila melanogaster. J Exp Biol 211(Pt 5):709–716PubMedCrossRefGoogle Scholar
  22. Steiger D, Fetchko M, Vardanyan A, Atanesyan L, Steiner K, Turski ML, Thiele DJ, Georgiev O, Schaffner W (2010) The Drosophila copper transporter Ctr1C functions in male fertility. J Biol Chem 285(22):17089–17097PubMedCrossRefGoogle Scholar
  23. Tauber E, Zordan M, Sandrelli F, Pegoraro M, Osterwalder N, Breda C, Daga A, Selmin A, Monger K, Benna C, Rosato E, Kyriacou CP, Costa R (2007) Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316(5833):1895–1898PubMedCrossRefGoogle Scholar
  24. van den Berghe PV, Klomp LW (2009) New developments in the regulation of intestinal copper absorption. Nutr Rev 67(11):658–672PubMedCrossRefGoogle Scholar
  25. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets—iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182(1):49–84PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2011

Authors and Affiliations

  1. 1.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK

Personalised recommendations