1887

Abstract

sp. A2 is a novel Gram-negative sulfate-reducing bacterium that was isolated from sediments of the Norilsk mining/smelting area in Russia. The organism possesses a monocistronic operon encoding a 71 kDa periplasmic multicopperoxidase, which we call DA2_CueO. Histidine-tagged DA2_CueO expressed from a plasmid in and purified by Ni–NTA affinity chromatography oxidizes Cu and Fe, and exhibits phenol oxidase activity with 2,2-azino-bis(3-ethylbenzthiazoline-6-sulphonic acid), 2,3-dihydroxybenzoic acid and 2,6-dimethoxyphenol as substrates, using O as the oxidant. When expressed in an knock-out strain, DA2_CueO exhibits phenol oxidase activity and enhances the copper tolerance of the strain. These findings indicate that the gene of sp. A2 encodes a multicopperoxidase with a role in metal ion resistance. The enzyme displays some novel structural features, which are discussed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000509
2017-08-01
2024-03-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/8/1229.html?itemId=/content/journal/micro/10.1099/mic.0.000509&mimeType=html&fmt=ahah

References

  1. Grass G, Fan B, Rosen BP, Lemke K, Schlegel HG et al. NreB from Achromobacter xylosoxidans 31A is a nickel-induced transporter conferring nickel resistance. J Bacteriol 2001; 183:2803–2807 [View Article][PubMed]
    [Google Scholar]
  2. Solioz M, Abicht HK, Mermod M, Mancini S. Response of Gram-positive bacteria to copper stress. J Biol Inorg Chem 2010; 15:3–14 [View Article][PubMed]
    [Google Scholar]
  3. Abicht HK, Gonskikh Y, Gerber SD, Solioz M. Non-enzymic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis IL1403. Microbiology 2013; 159:1190–1197 [View Article][PubMed]
    [Google Scholar]
  4. Raimunda D, González-Guerrero M, Leeber BW, Argüello JM. The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function. Biometals 2011; 24:467–475 [View Article][PubMed]
    [Google Scholar]
  5. Solioz M, Mancini S, Abicht HK, Mermod M. The lactic acid bacteria response to metal stress. In Tsakalidou E, Papadimitriou K. (editors) Stress Response of Lactic Acid Bacteria Heidelberg: Springer; 2011 pp. 163–195 [CrossRef]
    [Google Scholar]
  6. Kimura T, Nishioka H. Intracellular generation of superoxide by copper sulphate in Escherichia coli. Mutat Res 1997; 389:237–242 [View Article][PubMed]
    [Google Scholar]
  7. Changela A, Chen K, Xue Y, Holschen J, Outten CE et al. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 2003; 301:1383–1387 [View Article][PubMed]
    [Google Scholar]
  8. Macomber L, Imlay JA. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 2009; 106:8344–8349 [View Article][PubMed]
    [Google Scholar]
  9. Macomber L, Rensing C, Imlay JA. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 2007; 189:1616–1626 [View Article][PubMed]
    [Google Scholar]
  10. Chillappagari S, Seubert A, Trip H, Kuipers OP, Marahiel MA et al. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J Bacteriol 2010; 192:2512–2524 [View Article][PubMed]
    [Google Scholar]
  11. Azzouzi A, Steunou AS, Durand A, Khalfaoui-Hassani B, Bourbon ML et al. Coproporphyrin III excretion identifies the anaerobic coproporphyrinogen III oxidase HemN as a copper target in the Cu+-ATPase mutant copA of Rubrivivax gelatinosus. Mol Microbiol 2013; 88:339–351 [View Article][PubMed]
    [Google Scholar]
  12. Fung DK, Lau WY, Chan WT, Yan A. Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis. J Bacteriol 2013; 195:4556–4568 [View Article][PubMed]
    [Google Scholar]
  13. Foster AW, Dainty SJ, Patterson CJ, Pohl E, Blackburn H et al. A chemical potentiator of copper-accumulation used to investigate the iron-regulons of Saccharomyces cerevisiae. Mol Microbiol 2014; 93:317–330 [View Article][PubMed]
    [Google Scholar]
  14. Park HJ, Nguyen TT, Yoon J, Lee C. Role of reactive oxygen species in Escherichia coli inactivation by cupric ion. Environ Sci Technol 2012; 46:11299–11304 [View Article][PubMed]
    [Google Scholar]
  15. Chaturvedi KS, Henderson JP. Pathogenic adaptations to host-derived antibacterial copper. Front Cell Infect Microbiol 2014; 4:3 [View Article][PubMed]
    [Google Scholar]
  16. Rensing C, Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 2003; 27:197–213 [View Article][PubMed]
    [Google Scholar]
  17. Outten FW, Outten CE, Hale J, O'Halloran TV. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, CueR. J Biol Chem 2000; 275:31024–31029 [View Article][PubMed]
    [Google Scholar]
  18. Mancini S, Abicht HK, Karnachuk OV, Solioz M. Genome sequence of Desulfovibrio sp. A2, a highly copper resistant, sulfate-reducing bacterium isolated from effluents of a zinc smelter at the Urals. J Bacteriol 2011; 193:6793–6794 [View Article][PubMed]
    [Google Scholar]
  19. Giedroc DP, Arunkumar AI. Metal sensor proteins: nature's metalloregulated allosteric switches. Dalton Trans 20073107–3120 [View Article][PubMed]
    [Google Scholar]
  20. Boal AK, Rosenzweig AC. Structural biology of copper trafficking. Chem Rev 2009; 109:4760–4779 [View Article][PubMed]
    [Google Scholar]
  21. Kim EH, Nies DH, Mcevoy MM, Rensing C. Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 2011; 193:2381–2387 [View Article][PubMed]
    [Google Scholar]
  22. Padilla-Benavides T, George Thompson AM, Mcevoy MM, Argüello JM. Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J Biol Chem 2014; 289:20492–20501 [View Article][PubMed]
    [Google Scholar]
  23. Rowland JL, Niederweis M. A multicopper oxidase is required for copper resistance in Mycobacterium tuberculosis. J Bacteriol 2013; 195:3724–3733 [View Article][PubMed]
    [Google Scholar]
  24. Grass G, Rensing C. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun 2001; 286:902–908 [View Article][PubMed]
    [Google Scholar]
  25. Grass G, Thakali K, Klebba PE, Thieme D, Müller A et al. Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J Bacteriol 2004; 186:5826–5833 [View Article][PubMed]
    [Google Scholar]
  26. White C, Sayer JA, Gadd GM. Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination. FEMS Microbiol Rev 1997; 20:503–516 [View Article][PubMed]
    [Google Scholar]
  27. Karnachuk OV, Sasaki K, Gerasimchuk AL, Sukhanova O, Ivasenko DA et al. Precipitation of cu-sulfides by copper-tolerant Desulfovibrio isolates. Geomicrobiol J 2008; 25:219–227 [View Article]
    [Google Scholar]
  28. Karnachuk OV, Pimenov NV, Yusupov SK, Frank YA, Frank YA et al. Sulfate reduction potential in sediments in the Norilsk Mining area, Northern Siberia. Geomicrobiol J 2005; 22:11–25 [View Article]
    [Google Scholar]
  29. Ausubel RM, Brent R, Kingston RE, Moore DD, Smith JA et al. Current Protocols in Molecular Biology John Wiley & Sons, Inc; 1995
    [Google Scholar]
  30. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685 [View Article][PubMed]
    [Google Scholar]
  31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–254 [View Article][PubMed]
    [Google Scholar]
  32. Dagley S, Evans WC, Ribbons DW. New pathways in the oxidative metabolism of aromatic compounds by microorganisms. Nature 1960; 188:560–566 [View Article][PubMed]
    [Google Scholar]
  33. Djoko KY, Chong LX, Wedd AG, Xiao Z. Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. J Am Chem Soc 2010; 132:2005–2015 [View Article][PubMed]
    [Google Scholar]
  34. Steiner M, Lazaroff N. Direct method for continuous determination of iron oxidation by autotrophic bacteria. Appl Microbiol 1974; 28:872–880[PubMed]
    [Google Scholar]
  35. Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT et al. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 2002; 99:2766–2771 [View Article][PubMed]
    [Google Scholar]
  36. Zeng J, Lin X, Zhang J, Li X, Wong MH. Oxidation of polycyclic aromatic hydrocarbons by the bacterial laccase CueO from E. coli. Appl Microbiol Biotechnol 2011; 89:1841–1849 [View Article][PubMed]
    [Google Scholar]
  37. Jalalirad R. Selective and efficient extraction of recombinant proteins from the periplasm of Escherichia coli using low concentrations of chemicals. J Ind Microbiol Biotechnol 2013; 40:1117–1129 [View Article][PubMed]
    [Google Scholar]
  38. Witholt B, Boekhout M, Brock M, Kingma J, Heerikhuizen HV et al. An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal Biochem 1976; 74:160–170 [View Article][PubMed]
    [Google Scholar]
  39. Solomon EI, Sundaram UM, Machonkin TE. Multicopper oxidases and oxygenases. Chem Rev 1996; 96:2563–2606 [View Article][PubMed]
    [Google Scholar]
  40. Li X, Wei Z, Zhang M, Peng X, Yu G et al. Crystal structures of E. coli laccase CueO at different copper concentrations. Biochem Biophys Res Commun 2007; 354:21–26 [View Article][PubMed]
    [Google Scholar]
  41. Kim C, Lorenz WW, Hoopes JT, Dean JF. Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J Bacteriol 2001; 183:4866–4875 [View Article][PubMed]
    [Google Scholar]
  42. Singh SK, Grass G, Rensing C, Montfort WR. Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 2004; 186:7815–7817 [View Article][PubMed]
    [Google Scholar]
  43. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C et al. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 1998; 17:3640–3650 [View Article][PubMed]
    [Google Scholar]
  44. Hullo MF, Moszer I, Danchin A, Martin-Verstraete I. CotA of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 2001; 183:5426–5430 [View Article][PubMed]
    [Google Scholar]
  45. Wu T, Wang S, Wang Z, Peng X, Lu Y et al. A multicopper oxidase contributes to the copper tolerance of Brucella melitensis 16M. FEMS Microbiol Lett 2015; 362:1–7 [View Article]
    [Google Scholar]
  46. Stolle P, Hou B, Brüser T. The tat substrate CueO is transported in an incomplete folding state. J Biol Chem 2016; 291:13520–13528 [View Article][PubMed]
    [Google Scholar]
  47. Sakurai T, Kataoka K. Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 2007; 7:220–229 [View Article][PubMed]
    [Google Scholar]
  48. Cortes L, Wedd AG, Xiao Z. The functional roles of the three copper sites associated with the methionine-rich insert in the multicopper oxidase CueO from E. coli. Metallomics 2015; 7:776–785 [View Article][PubMed]
    [Google Scholar]
  49. Singh SK, Roberts SA, Mcdevitt SF, Weichsel A, Wildner GF et al. Crystal structures of multicopper oxidase CueO bound to copper(I) and silver(I): functional role of a methionine-rich sequence. J Biol Chem 2011; 286:37849–37857 [View Article][PubMed]
    [Google Scholar]
  50. Marshall B, Stintzi A, Gilmour C, Meyer JM, Poole K. Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter. Microbiology 2009; 155:305–315 [View Article][PubMed]
    [Google Scholar]
  51. Lobo SA, Almeida CC, Carita JN, Teixeira M, Saraiva LM. The haem-copper oxygen reductase of Desulfovibrio vulgaris contains a dihaem cytochrome c in subunit II. Biochim Biophys Acta 2008; 1777:1528–1534 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000509
Loading
/content/journal/micro/10.1099/mic.0.000509
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error