Applied Microbiology and Biotechnology

, Volume 98, Issue 18, pp 8005–8015 | Cite as

Copper tolerance in Frankia sp. strain EuI1c involves surface binding and copper transport

  • Medhat Rehan
  • Teal Furnholm
  • Ryan H. Finethy
  • Feixia Chu
  • Gomaah El-Fadly
  • Louis S. Tisa
Environmental biotechnology


Several Frankia strains have been shown to be copper-tolerant. The mechanism of their copper tolerance was investigated for Frankia sp. strain EuI1c. Copper binding was shown by binding studies. Unusual globular structures were observed on the surface of the bacterium. These globular structures were composed of aggregates containing many relatively smaller “leaf-like” structures. Scanning electron microscopy with energy-dispersive X-ray (SEM-EDAX) analysis of these structures indicated elevated copper and phosphate levels compared to the control cells. Fourier transform infrared spectroscopy (FTIR) analysis indicated an increase in extracellular phosphate on the cell surface of copper-stressed cells. Bioinformatics’ analysis of the Frankia sp. strain EuI1c genome revealed five potential cop genes: copA, copZ, copC, copCD, and copD. Experiments with Frankia sp. strain EuI1c using qRT-PCR indicated an increase in messenger RNA (mRNA) levels of the five cop genes upon Cu2+ stress. After 5 days of Cu2+ stress, the copA, copZ, copC, copCD, and copD mRNA levels increased 25-, 8-, 18-, 18-, and 25-fold, respectively. The protein profile of Cu2+-stressed Frankia sp. strain EuI1c cells revealed the upregulation of a 36.7 kDa protein that was identified as FraEuI1c_1092 (sulfate-binding periplasmic transport protein). Homologues of this gene were only present in the genomes of the Cu2+-resistant Frankia strains (EuI1c, DC12, and CN3). These data indicate that copper tolerance by Frankia sp. strain EuI1c involved the binding of copper to the cell surface and transport proteins.


Actinorhizal symbiosis Nitrogen fixation Metal resistance Soil microbe Bioremediation 



This investigation was supported, in part, by the New Hampshire Agricultural Experiment Station (NH00585 and NH00567), NSF CLF 1307367, and by the College of Life Science and Agriculture at the University of New Hampshire, Durham. This is scientific contribution number 2511 from the NH Agricultural Experiment Station. MR was supported by an Egyptian Channel Fellowship from The Egyptian Cultural Affairs and Missions Sectors. We thank Robert Mooney for his help with the photography, Nancy Chemin for her help with the electron microscopy, and Nicholas Beauchemin, Rebecca Wagers, Joel Richards, Scott Powers, and Glenn Krumholz for their initial contributions to this project.

Supplementary material

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ESM 1 (PDF 424 kb)


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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Medhat Rehan
    • 1
    • 2
  • Teal Furnholm
    • 1
  • Ryan H. Finethy
    • 1
  • Feixia Chu
    • 1
  • Gomaah El-Fadly
    • 2
  • Louis S. Tisa
    • 1
  1. 1.Department of Molecular, Cellular, and Biomedical SciencesUniversity of New HampshireDurhamUSA
  2. 2.Department of GeneticsKafrelsheikh UniversityKafr El-SheikhEgypt

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