Skip to main content
Log in

Cyanobacterial metallothioneins: Biochemistry and molecular genetics

  • Published:
Journal of Industrial Microbiology

Summary

Metallothioneins have been extensively studied in many different eukaryotes where they sequester, and hence detoxify, excess amounts of certain metal ions. However, the precise functions of many of these molecules are not fully understood. This article reviews literature concerning their namesakes in prokaryotes.

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

MT:

metallothionein

MRE:

metal regulatory element

References

  1. Bremner, I. 1991. Nutritional and physiologic significance of metallothionein. Methods Enzymol. 205: 25–35.

    PubMed  Google Scholar 

  2. Chubatsu, L.S., and R. Meneghini. 1993. Metallothionein protects DNA from oxidative damage. Biochem. J. 291: 193–198.

    PubMed  Google Scholar 

  3. Compere, S.J. and R.D. Palmiter. 1981. DNA methylation controls the inducibility of the mouse metallothionein-I gene in lymphoid cells. Cell 25: 233–240.

    PubMed  Google Scholar 

  4. Cozens, A.L. and J.E. Walker. 1987. The organization and sequence of the genes for ATP synthase subunits in the cyanobacteriumSynechococcus 6301: support for an endosymbiotic origin of chloroplasts. J. Mol. Biol. 194:359–383.

    PubMed  Google Scholar 

  5. Crawford, B.D., M.D. Enger, B.B. Griffith, J.K. Griffith, J.L. Hanners, J.L. Longmire, A.C. Munk, R.L. Stallings, J.G. Tesmer, R.A. Walters and C.E. Hildebrand. 1985. Coordinate amplification of metallothionein I and II genes in cadmium-resistant chinese hamster cells: implications for mechanisms regulating metallothionein gene expression. Mol. Cell. Biol. 5: 320–329.

    PubMed  Google Scholar 

  6. Dodd, I.B. and J.B. Egan. 1990. Improved detection of helix-turnhelix DNA-binding motifs in protein sequences. Nucleic Acids Res. 18:5019–5027.

    PubMed  Google Scholar 

  7. Durnam, D.M. and R.D. Palmiter. 1984. Induction of metallothionein-I messenger RNA in cultured cells by heavy metals and iodoacetate: evidence for gratuitous inducers. Mol. Cell. Biol. 4: 484–491.

    PubMed  Google Scholar 

  8. Fogel, S., J.W. Welch and M. Karin. 1983. Gene amplification in yeast:CUP1 copy number regulates copper resistance. Curr. Genet. 7:1–9.

    Google Scholar 

  9. Fowler, B.A., C.E. Hildebrand, Y. Kojima and M. Webb. 1987. Nomenclature of metallothionein. Experientia Suppl. 52: 19–22.

    PubMed  Google Scholar 

  10. Fürst, P., S. Hu, R. Hackett and D.H. Hamer. 1988. Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell 55: 705–717.

    PubMed  Google Scholar 

  11. Gupta, A., A.P. Morby, J.S. Turner, B.A. Whitton and N.J. Robinson. 1993. Deletion within the metallothionein locus of Cd-tolerantSynechococcus PCC 6301 involving a highly iterated palindrome (HIP1). Mol. Microbiol. 7: 189–195.

    Google Scholar 

  12. Gupta, A., B.A. Whitton, A.P. Morby, J.W. Huckle and N.J. Robinson: 1992. Amplification and rearrangement of a prokaryotic metallothionein locussmt inSynechococcus PCC 6301 selected for tolerance to cadmium. Proc. R. Soc. Lond. B 248: 273–281.

    Google Scholar 

  13. Hamer, D.H. 1986: Metallothionein. Annu. Rev. Biochem. 55: 913–951.

    PubMed  Google Scholar 

  14. Higham, D.P., P.J. Sadler and M.D. Scawen. 1984: Cadmium-resistantPseudomonas putida synthesizes novel cadmium binding proteins. Science 225:1043–1046.

    Google Scholar 

  15. Huckle, J.W. 1993. Prokaryotic metallothionein isolation, nucleotide sequence and expression. Ph.D. Thesis, University of Durham.

  16. Huckle, J.W., A.P. Morby, J.S. Turner and N.J. Robinson. 1993. Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol. Microbiol. 7: 177–187.

    PubMed  Google Scholar 

  17. Jackson, P.J., P.J. Unkefer, E. Delhaize and N.J. Robinson. 1990. Mechanisms of trace metal tolerance in plants. In: Environmental Injury to Plants (Katterman, F., ed.), pp. 231–255, Academic Press, San Diego.

    Google Scholar 

  18. Ji, G. and S. Silver. 1992. Regulation and expression of the arsenic resistance operon fromStaphylococcus aureus plasmid pI258. J. Bacteriol: 174: 3684–3694.

    PubMed  Google Scholar 

  19. Kägi, J.H.R. 1991. Overview of metallothionein. Methods Enzymol. 205: 613–626.

    PubMed  Google Scholar 

  20. Kägi, J.H.R. and Y. Kojima. 1987. Chemistry and biochemistry of metallothionein. Experientia Suppl. 52: 25–61.

    PubMed  Google Scholar 

  21. Kägi, J.H.R. and A. Schäffer. 1988. Biochemistry of metallothionein. Biochemistry 27: 8509–8515.

    PubMed  Google Scholar 

  22. Kägi, J.H.R. and B.L. Vallee. 1960. Metallothionein: a cadmium and zinc-containing protein from the equine renal cortex. J. Biol. Chem. 235: 3460–3465.

    PubMed  Google Scholar 

  23. Karin, M. 1985. Metallothioneins: proteins in search of function. Cell 41:9–10.

    PubMed  Google Scholar 

  24. Karin, M., R. Najarian, A. Haslinger, P. Valenzuela, J. Welsh and S. Fogel. 1984. Primary structure and transcription of an amplified genetic locus: the CUP1 locus of yeast. Proc. Natl. Acad. Sci. USA 81: 337–341.

    PubMed  Google Scholar 

  25. Kojima, Y. 1991. Definitions and nomenclature of metallothioneins. Methods Enzymol. 205: 8–10.

    PubMed  Google Scholar 

  26. Labbé, S., J. Prevost, P. Remondelli, A. Leone and C. Séguin. 1991. A nuclear factor binds to the metal regulatory elements of the mouse gene encoding metallothionein-1. Nucleic Acids Res. 19: 4225–4231.

    PubMed  Google Scholar 

  27. Luisi, B. 1992. Zinc standard for the economy. Nature 356: 379–380.

    PubMed  Google Scholar 

  28. Mack Ivey, D., A.A. Guffanti, Z. Shen, N. Kudyan and T.A. Krulwich. 1992. ThecadC gene product of alkaliphilicBacillus firmus OF4 partially restores Na+ resistance to anEscherichia coli strain lacking an Na+/H+ antiporter (NhaA). J. Bacteriol. 174: 4878–4884.

    PubMed  Google Scholar 

  29. Maclean, F.I., O.J. Lucis, Z.A. Shakh and E.R. Jansz. 1972. The uptake and subcellular distribution of Cd and Zn in microorganisms. Fed. Proc. 31: 699.

    Google Scholar 

  30. Margoshes, M. and B.L. Vallee. 1957. A cadmium protein from equine kidney cortex. J. Am. Chem. Soc. 79: 4813–4814.

    Google Scholar 

  31. Masters, B.A., E.J. Kelly, C.J. Quaife, R.L. Brinster and R.D. Palmiter. 1994. Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc. Natl. Acad. Sci. USA 91: 584–588.

    PubMed  Google Scholar 

  32. Mehra, R.K., J.R. Garey and D.R. Winge. 1990. Selective and tandem amplification of a member of the metallothionein gene family inCandida glabrata. J. Biol. Chem. 265: 6369–6375.

    PubMed  Google Scholar 

  33. Morby, A.P., J.S. Turner, J.W. Huckle and N.J. Robinson. 1993. SmtB is a metal regulated repressor of the cyanobacterial metallothionein genesmtA: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res. 21: 921–925.

    PubMed  Google Scholar 

  34. Münger, K., U.A. Germann and K. Lerch. 1987. TheNeurospora crassa metallothionein gene. J. Biol. Chem. 262: 7363–7367.

    PubMed  Google Scholar 

  35. Münger, K. and K. Lerch. 1985: Copper metallothionein from the fungusAgaricus bisporus: chemical and spectroscopic properties. Biochemistry 24:6751–6756.

    Google Scholar 

  36. Olafson, R.W. 1984. Prokaryotic metallothionein. Int. J. Pept. Protein Res. 24: 303–308.

    Google Scholar 

  37. Olafson, R.W. 1986. Physiological and chemical characterization of cyanobacterial metallothioneins. Environ. Health Perspect. 65: 71–75.

    PubMed  Google Scholar 

  38. Olafson, R.W. 1991. Purification of prokaryotic metallothioneins. Methods Enzymol. 205: 283–286.

    PubMed  Google Scholar 

  39. Olafson, R.W., K. Abel and R.G. Sim. 1979. Prokaryotic metallothionein: preliminary characterization of a blue green alga heavy metal binding protein. Biochem. Biophys. Res. Commun. 89: 36–43.

    PubMed  Google Scholar 

  40. Olafson, R.W., S. Loya and R.G. Sim. 1980. Physiological parameters of prokaryotic metallothionein induction. Biochem. Biophys. Res. Commun. 95: 1495–1503.

    PubMed  Google Scholar 

  41. Olfason, R.W., W.D. McCubbin and C.M. Kay. 1988. Primaryand secondary-structural analysis of a unique prokaryotic metallothionein from aSynechococcus sp. cyanobacterium. Biochem. J. 251: 691–699.

    PubMed  Google Scholar 

  42. Palmiter, R.D. 1987. Molecular biology of metallothionein gene expression. Experientia Suppl. 52: 63–80.

    PubMed  Google Scholar 

  43. Radtke, F., R. Heuchel, O. Georgiev, M. Hergersberg, M. Gariglio, Z. Dembic and W. Schaffner 1993. Cloned transcription factor MTF-1 activates the mouse metallothionein-I promoter. EMBO J. 12: 1355–1362.

    PubMed  Google Scholar 

  44. Rauser, W.E. 1990. Phytochelatins. Annu. Rev. Biochem. 59: 61–86.

    PubMed  Google Scholar 

  45. Robière, M.C., A.M. Castets, J. Houmard and N. Tandeau de Marsac. 1986. Plasmid distribution among unicellular and filamentous cyanobacteria: occurrence of large and mega-plasmids. FEMS Microbiol. Lett. 37: 269–275.

    Google Scholar 

  46. Robinson, N.J. 1990. Metal binding polypeptides in plants. In: Heavy Metal Tolerance in Plants: Evolutionary Aspects (Shaw, J.A., ed.), pp. 195–214, CRC Press, Boca Raton.

    Google Scholar 

  47. Robinson, N.J. and P.J. Jackson. 1986. ‘Metallothionein-like’ metal complexes in angiosperms: their structure and function. Plant Physiol. 67: 499–506.

    Google Scholar 

  48. Robinson, N.J., A.M. Tommey, C. Kuske and P.J. Jackson. 1993. Plant metallothioneins. Biochem. J. 295: 1–10.

    PubMed  Google Scholar 

  49. Robinson, N.J., A. Gupta, A.P. Fordham-Skelton, R.R.D. Croy, B.A. Whitton and J.W. Huckle. 1990. Prokaryotic metallothionein gene characterization and expression: chromosome crawling by ligation mediated PCR. Proc. R. Soc. Lond. B 242: 241–247.

    Google Scholar 

  50. San Francisco, M.J.D., C.L. Hope, J.B. Owolabi, L.S. Tisa and B.P. Rosen. 1990. Identification of the metalloregulatory element of the plasmid-encoded arsenical resistance operon. Nucleic Acids Res. 18: 619–624.

    PubMed  Google Scholar 

  51. Shi, J., W.P. Lindsay, J.W. Huckle, A.P. Morby and N.J. Robinson. 1992. Cyanobacterial metallothionein gene expressed inEscherichia coli—metal binding properties of the expressed protein. FEBS Lett. 303: 159–163.

    PubMed  Google Scholar 

  52. Shimizu, T., T. Hiyama, M. Ikeuchi and Y. Inoue. 1992. Nucleotide sequence of a metallothionein gene of the thermophilic cyanobacteriumSynechococcus vulcanus. Plant Mol. Biol. 20: 565–567.

    PubMed  Google Scholar 

  53. Silver, S. and M. Walderhaug. 1992. Gene regulation of plasmidand chromosome-determined inorganic ion transport in bacteria. Microbiol. Rev. 56: 195–228.

    PubMed  Google Scholar 

  54. Silver, S., G. Nucifora and L.T. Phung. 1993. Human Menkes X-chromosome disease and the staphylococcal cadmium-resistance ATPase: a remarkable similarity in protein sequences. Mol. Microbiol. 10: 7–12.

    PubMed  Google Scholar 

  55. Steffens, J.C. 1990. The heavy metal-binding peptides of plants. Plant Mol. Biol. 41: 553–575.

    Google Scholar 

  56. Takatera, K. and T. Watanabe. 1992. Application of high performance liquid chromatography/inductively coupled plasma mass spectrometry to the speciation of cadmium-binding metallothionein-like protein in a cyanobacterium. Anal. Sci. 8: 469–474.

    Google Scholar 

  57. Tamai, K.T., E.B. Gralla, L.M. Ellerby, J.S. Valentine and D.J. Thiele. 1993. Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc. Natl. Acad. Sci. USA 90: 8013–8017.

    PubMed  Google Scholar 

  58. Thiele, D.J., C.F. Wright, M.J. Walling and D.H. Hamer. 1987. Function and regulation of yeast copper thionein. Experientia Suppl. 52: 423–429.

    PubMed  Google Scholar 

  59. Thiele, D.J. 1992. Metal-regulated transcription in eukaryotes. Nucleic Acids Res. 20: 1183–1191.

    PubMed  Google Scholar 

  60. Tomsett, A.B. and D.A. Thurman. 1988. Molecular biology of metal tolerances of plants. Plant Cell Environ. 11: 383–394.

    Google Scholar 

  61. Turner, J.S. 1993. Functional analysis of the prokaryotic metallothionein locus,smt. Ph.D. Thesis, University of Durham.

  62. Turner, J.S., A.P. Morby, B.A. Whitton, A. Gupta and N.J. Robinson. 1993. Construction and characterization of Zn2+/Cd2+ hypersensitive cyanobacterial mutants lacking a functional metallothionein locus. J. Biol. Chem. 268: 4494–4498.

    PubMed  Google Scholar 

  63. Turner, J.S., N.J. Robinson and A. Gupta. 1994. Construction of Zn2+/Cd2+-tolerant cyanobacteria with a modified metallothionein divergon: Further analysis of the function and regulation ofsmt. J. Ind. Microbiol. 14: 258–263.

    Google Scholar 

  64. Vallee, B.L. 1991. Introduction to metallothionein. Methods Enzymol. 205: 3–7.

    PubMed  Google Scholar 

  65. Verma, S.K. and H.N. Singh. 1991. Evidence for energy-dependent copper efflux as a mechanisms of Cu2+ resistance in the cyanobacteriumNostoc calcicola. FEMS Microbiol. Lett. 84: 291–294.

    Google Scholar 

  66. Wu, J. and B.P. Rosen. 1993. Metalloregulated expression of the aureus cadA cadmium resistance determinant of plasmid p1258. J. Bacteriol. 173: 7636–7642.

    Google Scholar 

  67. Zeng, J., R. Heuchel, W. Schaffner and J.H.R. Kägi. 1991. Thionein (apometallothionein) can modulate DNA binding and transcription activation by zinc finger containing factor Sp1. FEBS Lett. 279: 310–312.

    PubMed  Google Scholar 

  68. Zeng, J., B.L. Vallee, and J.H.R. Kägi. 1991. Zinc transfer from transcription factor IIIA fingers to thionein clusters. Proc. Natl. Acad. Sci. USA 88: 9984–9988.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Turner, J.S., Robinson, N.J. Cyanobacterial metallothioneins: Biochemistry and molecular genetics. Journal of Industrial Microbiology 14, 119–125 (1995). https://doi.org/10.1007/BF01569893

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01569893

Key words

Navigation