Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.
Journal of Microbiology and Biotechnology
Condition  Expression
When you enter More than two words, please use ‘and , or’ operation by means of putting ‘,(Comma Mark)’ between each word.

2012 ; 22(6): 742~753

AuthorShee Ping Ng, Enzo A. Palombo, Mrinal Bhave
AffiliationEnvironment and Biotechnology Centre, Faculty of Life and Social Sciences, Swinburne University of Technology, PO Box 218, Melbourne, Victoria 3122, Australia
TitleThe Heavy Metal Tolerant Soil Bacterium Achromobacter sp. AO22 Contains a Unique Copper Homeostasis Locus and Two mer Operons
PublicationInfo J. Microbiol. Biotechnol.2012 ; 22(6): 742~753
AbstractCopper-containing compounds are introduced into the environment through agricultural chemicals, mining, and metal industries and cause severe detrimental effects on ecosystems. Certain microorganisms exposed to these stressors exhibit molecular mechanisms to maintain intracellular copper homeostasis and avoid toxicity. We have previously reported that the soil bacterial isolate Achromobacter sp. AO22 is multi-heavy metal tolerant and exhibits a mer operon associated with a Tn21 type transposon. The present study reports that AO22 also hosts a unique cop locus encoding copper homeostasis determinants. The putative cop genes were amplified from the strain AO22 using degenerate primers based on reported cop and pco sequences, and a constructed 10,552 base pair contig (GenBank Accession No. GU929214). BLAST analyses of the sequence revealed a unique cop locus of 10 complete open reading frames, designated copSRABGOFCDK, with unusual separation of copCD from copAB. The promoter areas exhibit two putative cop boxes, and copRS appear to be transcribed divergently from other genes. The putative protein CopA may be a copper oxidase involved in export to the periplasm, CopB is likely extracytoplasmic, CopC may be periplasmic, CopD is cytoplasmic/ inner membrane, CopF is a P-type ATPase, and CopG, CopO, and CopK are likely copper chaperones. CopA, B, C, and D exhibit several potential copper ligands and CopS and CopR exhibit features of two-component regulatory systems. Sequences flanking indicate the AO22 cop locus may be present within a genomic island. Achromobacter sp. strain AO22 is thus an ideal candidate for understanding copper homeostasis mechanisms and exploiting them for copper biosensor or biosorption systems.
Full-Text(PDF)
Supplemental Data
Keywordsheavy metals, copper, mer, cop, two component signal transduction, genomic island
References
  1. Adaikkalam, V. and S. Swarup. 2005. Characterization of copABCD operon from a copper-sensitive Pseudomonas putida strain. Can. J. Microbiol. 51: 209-216.
    Pubmed CrossRef
  2. Arnesano, F., L. Banci, I. Bertini, S. Mangani, and A. R. Thompsett. 2003. A redox switch in CopC: An intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites. Proc. Natl. Acad. Sci. USA 100: 3814-3819.
    Pubmed CrossRef Pubmed Central
  3. Basim, H., G. V. Minsavage, R. E. Stall, J.-F. Wang, S. Shanker, and J. B. Jones. 2005. Characterisation of a unique chromosomal copper resistance gene cluster from Xanthomonas campestris pv. vesicatoria. Appl. Environ. Microbiol. 71: 8284-8291.
    Pubmed CrossRef Pubmed Central
  4. Bersch, B., A. Favier, P. Schanda, S. van Aelst, T. Vallaeys, J. Covès, et al. 2008. Molecular structure and metal-binding properties of the periplasmic CopK protein expressed in Cupriavidus metallidurans CH34 during copper challenge. J. Mol. Biol. 380: 386-403.
    Pubmed CrossRef
  5. Bontidean, I., A. Mortari, S. Leth, N. L. Brown, U. Karlson, M. M. Larsen, et al. 2004. Biosensors for detection of mercury in contaminated soils. Environ. Pollut. 131: 255-262.
    Pubmed CrossRef
  6. Brown, N. L., S. R. Barrett, J. Camakaris, B. T. Lee, and D. A. Rouch. 1995. Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. Mol. Microbiol. 17: 1153-1166.
    Pubmed CrossRef
  7. Cha, J. S. and D. A. Cooksey. 1991. Copper resistance in Pseudomonas syringae mediated by periplasmic and outer membrane proteins. Proc. Natl. Acad. Sci. USA 88: 8915-8919.
    CrossRef
  8. Chen, S., E. Kim, M. L. Shuler, and D. B. Wilson. 1998. Hg2+ removal by genetically engineered Escherichia coli in a hollow fiber bioreactor. Biotechnol. Prog. 14: 667-671.
    Pubmed CrossRef
  9. Cooksey, D. A. 1993. Copper uptake and resistance in bacteria. Mol. Microbiol. 7: 1-5.
    Pubmed CrossRef
  10. Deng, X. and D. B. Wilson. 2001. Bioaccumulation of mercury from wastewater by genetically engineered Escherichia coli. Appl. Microbiol. Biotechnol. 56: 276-279.
    Pubmed CrossRef
  11. Diels, L., Q. Dong, D. van der Lelie, W. Baeyens, and M. Mergeay. 1995. The czc operon of Alcaligenes eutrophus CH34:From resistance mechanism to the removal of heavy metals. J. Ind. Microbiol. 14: 142-153.
    Pubmed CrossRef
  12. Djoko, K. Y., Z. Xiao, D. L. Huffman, and A. G. Wedd. 2007. Conserved mechanism of copper binding and transfer. A comparison of the copper-resistance proteins PcoC from Escherichia coli and CopC from Pseudomonas syringae. Inorg. Chem. 46:4560-4568.
    Pubmed CrossRef
  13. Djoko, K. Y., Z. Xiao, and A. G. Wedd. 2008. Copper resistance in E. coli: The multicopper oxidase PcoA catalyzes oxidation of copper(I) in CuICuII-PcoC. ChemBioChem 9: 1579-1582.
    Pubmed CrossRef
  14. Dorsey, A. and L. Ingerman. 2004. Toxicology Profile for Copper. Agency for Toxic Substances and Disease Registry.
  15. Figurski, D. H. and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76: 1648-1652.
    CrossRef
  16. Forst, S., J. Delgado, and M. Inouye. 1989. Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 6052-6056.
    CrossRef
  17. Grass, G. and C. Rensing. 2001. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem. Biophys. Res. Commun. 286: 902-908.
    Pubmed CrossRef
  18. Gupta, A., K. Matsui, J. F. Lo, and S. Silver. 1999. Molecular basis for resistance to silver cations in Salmonella. Nat. Med. 5:183-188.
    Pubmed CrossRef
  19. Harley, C. B. and R. P. Reynolds. 1987. Analysis of E. coli promoter sequences. Nucl. Acids Res. 15: 2343-2361.
    Pubmed CrossRef Pubmed Central
  20. Hettler, J., G. Irion, and B. Lehmann. 1997. Environmental impact of mining waste disposal on a tropical lowland river system: A case study on the Ok Tedi Mine, Papua New Guinea. Mineral. Depos. 32: 280-291.
    CrossRef
  21. Huang, C.-C., M. Narita, T. Yamagata, Y. Itoh, and G. Endo. 1999. Structure analysis of a class II transposon encoding the mercury resistance of the Gram-positive bacterium Bacillus megaterium MB1, a strain isolated from Minamata Bay, Japan. Gene 234: 361-369.
    CrossRef
  22. Huffman, D. L., J. Huyett, F. W. Outten, P. E. Doan, L. A. Finney, B. M. Hoffman, and T. V. O’Halloran. 2002. Spectroscopy of Cu(II)-PcoC and the multicopper oxidase function of PcoA, two essential components of Escherichia coli pco copper resistance operon. Biochemistry 41: 10046-10055.
    Pubmed CrossRef
  23. Kataoka, K., H. Komori, Y. Ueki, Y. Konno, Y. Kamitaka, S. Kurose, et al. 2007. Structure and function of the engineered multicopper oxidase CueO from Escherichia coli - deletion of the methionine-rich helical region covering the substrate-binding site. J. Mol. Biol. 373: 141-152.
    Pubmed CrossRef
  24. Kholodii, G., O. V. Yurieva, O. L. Lomovskaya, Z. Gorlenko, S. Z. Mindlin, and V. G. Nikiforov. 1993. Tn5053, a mercury resistance transposon with integron’s ends. J. Mol. Biol. 230:1103-1107.
    Pubmed CrossRef
  25. Lee, S. M., G. Grass, C. Rensing, S. R. Barrett, C. J. Yates, J. V. Stoyanov, and N. L. Brown. 2002. The Pco proteins are involved in periplasmic copper handling in Escherichia coli. Biochem. Biophys. Res. Commun. 295: 616-620.
    CrossRef
  26. Lee, Y. A., M. Hendson, N. J. Panopoulos, and M. N. Schroth. 1994. Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas campestris pv. juglandis: Homology with small blue copper proteins and multicopper oxidase. J. Bacteriol. 176: 173-188.
    Pubmed Pubmed Central
  27. Leedjarv, A., A. Ivask, and M. Virta. 2008. Interplay of different transporters in the mediation of divalent heavy metal resistance in Pseudomonas putida KT2440. J. Bacteriol. 190:2680-2689.
    Pubmed CrossRef Pubmed Central
  28. Lim, C. K. and D. A. Cooksey. 1993. Characterization of chromosomal homologs of the plasmid-borne copper resistance operon of Pseudomonas syringae. J. Bacteriol. 175: 4492-4498.
    Pubmed Pubmed Central
  29. Mellano, M. A. and D. A. Cooksey. 1988. Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. tomato. J. Bacteriol. 170: 2879-2883.
    Pubmed Pubmed Central
  30. Mergeay, M., S. Monchy, P. Janssen, R. Houdt, and N. Leys. 2009. Megaplasmids in Cupriavidus genus and metal resistance, pp. 209-238. In E. Schwartz (ed.). Microbial Megaplasmids. Springer, Berlin.
    CrossRef
  31. Mergeay, M., S. Monchy, T. Vallaeys, V. Auquier, A. Benotmane, P. Bertin, et al. 2003. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: Towards a catalogue of metal-responsive genes. FEMS Microbiol. Rev. 27: 385-410.
    CrossRef
  32. Mergeay, M., D. Nies, H. G. Schlegel, J. Gerits, P. Charles, and F. Van Gijsegem. 1985. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162: 328-334.
    Pubmed Pubmed Central
  33. Messerschmidt, A., R. Ladenstein, R. Huber, M. Bolognesi, L. Avigliano, R. Petruzzelli, et al. 1992. Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J. Mol. Biol. 224:179-205.
    CrossRef
  34. Mills, S. D., C. K. Lim, and D. A. Cooksey. 1994. Purification and characterization of CopR, a transcriptional activator protein that binds to a conserved domain (cop box) in copper-inducible promoters of Pseudomonas syringae. Mol. Gen. Genet. 244:341-351.
    CrossRef
  35. Monchy, S., M. A. Benotmane, R. Wattiez, S. van Aelst, V. Auquier, B. Borremans, et al. 2006. Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152:1765-1776.
    Pubmed CrossRef
  36. Multhaup, G., D. Strausak, K.-D. Bissig, and M. Solioz. 2001. Interaction of the CopZ copper chaperone with the CopA copper ATPase of Enterococcus hirae assessed by surface plasmon resonance. Biochem. Biophys. Res. Commun. 288: 172-177.
    Pubmed CrossRef
  37. Munson, G. P., D. L. Lam, F. W. Outten, and T. V. O’Halloran. 2000. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J. Bacteriol. 182:5864-5871.
    Pubmed CrossRef Pubmed Central
  38. Ng, S. P., B. Davis, E. A. Palombo, and M. Bhave. 2009. A Tn5051-like mer-containing transposon identified in a heavy metal tolerant strain Achromobacter sp. AO22. BMC Res. Notes 2: 38.
    Pubmed CrossRef Pubmed Central
  39. Outten, F. W., D. L. Huffman, J. A. Hale, and T. V. O’Halloran. 2001. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276: 30670-30677.
    Pubmed CrossRef
  40. Park, H., S. K. Saha, and M. Inouye. 1998. Two-domain reconstitution of a functional protein histidine kinase. Proc. Natl. Acad. Sci. USA 95: 6728-6732.
    CrossRef
  41. Rensing, C., B. Fan, R. Sharma, B. Mitra, and B. P. Rosen. 2000. CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 97: 652-656.
    CrossRef
  42. Rensing, C. and G. Grass. 2003. Escherichia coli mechanisms of copper homeostasis in a changing environment FEMS Microbiol. Rev. 27: 197-213.
    CrossRef
  43. Rouch, D. A. and N. L. Brown. 1997. Copper-inducible transcriptional regulation at two promoters in the Escherichia coli copper resistance determinant pco. Microbiology 143:1191-1202.
    Pubmed CrossRef
  44. Sarret, G., A. Favier, J. Coves, J.-L. Hazemann, M. Mergeay, and B. Bersch. 2010. CopK from Cupriavidus metallidurans CH34 binds Cu(I) in a tetrathioether site: Characterization by X-ray absorption and NMR spectroscopy. J. Am. Chem. Soc. 132: 3770-3777.
    Pubmed CrossRef
  45. Schleheck, D., T. P. Knepper, K. Fischer, and A. M. Cook. 2004. Mineralisation of individual congeners of linear alkylbenzenesulfonate by defined pairs of heterotrophic bacteria. Appl. Environ. Microbiol. 70: 4053-4063.
    Pubmed CrossRef Pubmed Central
  46. Solioz, M. and A. Odermatt. 1995. Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J. Biol. Chem. 270: 9217-9221.
    Pubmed CrossRef
  47. Stock, A. M., J. M. Mottonen, J. B. Stock, and C. E. Schutt. 1989. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature 337: 745-749.
    Pubmed CrossRef
  48. Teitzel, G. M. and M. R. Parsek. 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69: 2313-2320.
    Pubmed CrossRef Pubmed Central
  49. Teixeira, E. C., J. C. Franco de Oliveira, M. T. Marques Novo, and M. C. Bertolini. 2008. The copper resistance operon copAB from Xanthomonas axonopodis pathovar citri: Gene inactivation results in copper sensitivity. Microbiology 154: 402-412.
    Pubmed CrossRef
  50. Trajanovska, S., M. L. Britz, and M. Bhave. 1997. Detection of heavy metal ion resistance genes in Gram-positive and Gramnegative bacteria isolated from a lead-contaminated site. Biodegradation 8: 113-124.
    Pubmed CrossRef
  51. Van Houdt, R., S. Monchy, N. Leys, and M. Mergeay. 2009. New mobile genetic elements in Cupriavidus metallidurans CH34, their possible roles and occurrence in other bacteria. Antonie Van Leeuwenhoek 96: 205-226.
    Pubmed CrossRef
  52. Voloudakis, A. E., T. M. Reignier, and D. A. Cooksey. 2005. Regulation of resistance to copper in Xanthomonas axonopodis pv. vesicatoria. Appl. Environ. Microbiol. 71: 782-789.
    Pubmed CrossRef Pubmed Central
  53. Yamamoto, K. and A. Ishihama. 2005. Transcriptional response of Escherichia coli to external copper. Mol. Microbiol. 56:215-227.
    Pubmed CrossRef
  54. Zhang, L., M. Koay, M. J. Maher, Z. Xiao, and A. G. Wedd. 2006. Intermolecular transfer of copper ions from the CopC protein of Pseudomonas syringae. Crystal structures of fully loaded CuICuII forms. J. Am. Chem. Soc. 128: 5834-5850.
    Pubmed CrossRef
Copyright © 2009 by the Korean Society for Microbiology and Biotechnology.
All right reserved. Mail to jmb@jmb.or.kr
Online ISSN: 1738-8872    Print ISSN: 1017-7825    Powered by INFOrang.co., Ltd