Skip to main content
SpringerLink
Log in

Metal Response in Cupriavidus metallidurans: Insights into the Structure-Function Relationship of Proteins

  • Chapter
  • First Online:
Metal Response in Cupriavidus metallidurans

Part of the book series: SpringerBriefs in Molecular Science ((SB BIOMETALS))

Abstract

Bacteria such as Cupriavidus metallidurans have developed different strategies for tolerating toxic levels of metal ions. Metal ion resistance requires the contribution of multiple layers of mechanisms, the most efficient being the efflux of the noxious cations out of the cell regulated by transport systems. Structural and functional data from bacterial primary and secondary transporters are outlined and detailed for the corresponding C.metallidurans proteins. Next, the available high-resolution three-dimensional structures of C. metallidurans proteins involved in metal resistance mechanisms are reviewed and their structure-function relationship is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abuzaid A, Hamouda A, Amyes SG (2012) Klebsiella pneumoniae susceptibility to biocides and its association with cepA, qacΔE and qacE efflux pump genes and antibiotic resistance. J Hosp Infect 81(2):87–91

    CAS  Google Scholar 

  • Aguilera S, Aguilar ME, Chavez MP, Lopez-Meza JE, Pedraza-Reyes M, Campos-Garcia J, Cervantes C (2004) Essential residues in the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol Lett 232(1):107–112

    CAS  Google Scholar 

  • Aires JR, Nikaido H (2005) Aminoglycosides are captured from both periplasm and cytoplasm by the AcrD multidrug efflux transporter of Escherichia coli. J Bacteriol 187(6):1923–1929

    CAS  Google Scholar 

  • Akama H, Kanemaki M, Yoshimura M, Tsukihara T, Kashiwagi T, Yoneyama H, Narita S, Nakagawa A, Nakae T (2004a) Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: dual modes of membrane anchoring and occluded cavity end. J Biol Chem 279(51):52816–52819

    CAS  Google Scholar 

  • Akama H, Matsuura T, Kashiwagi S, Yoneyama H, Narita S, Tsukihara T, Nakagawa A, Nakae T (2004b) Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J Biol Chem 279(25):25939–25942

    CAS  Google Scholar 

  • Albers RW (1967) Biochemical aspects of active transport. Annu Rev Biochem 36:727–756

    CAS  Google Scholar 

  • Alberts IL, Nadassy K, Wodak SJ (1998) Analysis of zinc binding sites in protein crystal structures. Protein Sci 7(8):1700–1716

    CAS  Google Scholar 

  • Alvarez AH, Moreno-Sanchez R, Cervantes C (1999) Chromate efflux by means of the ChrA chromate resistance protein from Pseudomonas aeruginosa. J Bacteriol 181(23):7398–7400

    CAS  Google Scholar 

  • Anastassopoulou I, Banci L, Bertini I, Cantini F, Katsari E, Rosato A (2004) Solution structure of the apo and copper(I)-loaded human metallochaperone HAH1. Biochemistry 43(41):13046–13053

    CAS  Google Scholar 

  • Andersen C, Koronakis E, Bokma E, Eswaran J, Humphreys D, Hughes C, Koronakis V (2002) Transition to the open state of the TolC periplasmic tunnel entrance. Proc Natl Acad Sci USA 99(17):11103–11108

    CAS  Google Scholar 

  • Andersson M, Bondar AN, Freites JA, Tobias DJ, Kaback HR, White SH (2012) Proton-coupled dynamics in lactose permease. Structure 20(11):1893–1904

    CAS  Google Scholar 

  • Anton A (2001) Genetische und biochemische charakterisierung von CzcD und anderen regulatoren der czc-vermittelten schwermetallresistenz in Ralstonia metallidurans. Martin-Luther-Universität Halle-Wittenberg, Halle

    Google Scholar 

  • Anton A, Grosse C, Reissmann J, Pribyl T, Nies DH (1999) CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J Bacteriol 181(22):6876–6881

    CAS  Google Scholar 

  • Anton A, Weltrowski A, Haney CJ, Franke S, Grass G, Rensing C, Nies DH (2004) Characteristics of zinc transport by two bacterial cation diffusion facilitators from Ralstonia metallidurans CH34 and Escherichia coli. J Bacteriol 186(22):7499–7507

    CAS  Google Scholar 

  • Argüello JM (2003) Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J Membr Biol 195(2):93–108

    Google Scholar 

  • Argüello JM, Eren E, Gonzalez-Guerrero M (2007) The structure and function of heavy metal transport P1B-ATPases. Biometals 20(3–4):233–248

    Google Scholar 

  • Argüello JM, Gonzalez-Guerrero M, Raimunda D (2011) Bacterial transition metal P(1B)-ATPases: transport mechanism and roles in virulence. Biochemistry 50(46):9940–9949

    Google Scholar 

  • Arnesano F, Banci L, Bertini I, Huffman DL, O’Halloran TV (2001) Solution structure of the Cu(I) and apo forms of the yeast metallochaperone, Atx1. Biochemistry 40(6):1528–1539

    CAS  Google Scholar 

  • Arnesano F, Banci L, Bertini I, Mangani S, Thompsett AR (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(7):3814–3819

    CAS  Google Scholar 

  • Ash M-R, Chong LX, Maher MJ, Hinds MG, Xiao Z, Wedd AG (2011) Molecular basis of the cooperative binding of Cu(I) and Cu(II) to the CopK protein from Cupriavidus metallidurans CH34. Biochemistry 50:9237–9247

    CAS  Google Scholar 

  • Auld DS (2005) Zinc Enzymes. In: King RB (ed) Encyclopedia of inorganic and bioinorganic chemistry. Wiley, Chichester, pp 5885–5927

    Google Scholar 

  • Auld DS (2009) The ins and outs of biological zinc sites. Biometals 22(1):141–148

    CAS  Google Scholar 

  • Auquier V (2006) Identification et caractérisation de protéines membranaires impliquées dans les systèmes de résistance aux métaux lourds chez Cupriavidus metallidurans CH34. Université Libre de Bruxelles, Brussels

    Google Scholar 

  • Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46(1):84–101

    CAS  Google Scholar 

  • Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K (2006) A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 188(8):2761–2773

    CAS  Google Scholar 

  • Bagai I, Liu W, Rensing C, Blackburn NJ, McEvoy MM (2007) Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system. J Biol Chem 282(49):35695–35702

    CAS  Google Scholar 

  • Bagai I, Rensing C, Blackburn NJ, McEvoy MM (2008) Direct metal transfer between periplasmic proteins identifies a bacterial copper chaperone. Biochemistry 47(44):11408–11414

    CAS  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14(4):176–182

    CAS  Google Scholar 

  • Banci L, Bertini I, Del Conte R, Markey J, Ruiz-Duenas FJ (2001) Copper trafficking: the solution structure of Bacillus subtilis CopZ. Biochemistry 40(51):15660–15668

    CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S, D’Onofrio M, Gonnelli L, Marhuenda-Egea FC, Ruiz-Duenas FJ (2002a) Solution structure of the N-terminal domain of a potential copper-translocating P-type ATPase from Bacillus subtilis in the apo and Cu(I) loaded states. J Mol Biol 317(3):415–429

    CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S, Finney LA, Outten CE, O’Halloran TV (2002b) A new zinc-protein coordination site in intracellular metal trafficking: solution structure of the Apo and Zn(II) forms of ZntA(46-118). J Mol Biol 323(5):883–897

    CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S (2009) Copper trafficking in biology: an NMR approach. Hfsp Journal 3(3):165–175

    CAS  Google Scholar 

  • Bavro VN, Pietras Z, Furnham N, Perez-Cano L, Fernandez-Recio J, Pei XY, Misra R, Luisi B (2008) Assembly and channel opening in a bacterial drug efflux machine. Mol Cell 30(1):114–121

    CAS  Google Scholar 

  • Bersch B, Favier A, Schanda P, van Aelst S, Vallaeys T, Covès J, Mergeay M, Wattiez R (2008) Molecular structure and metal-binding properties of the periplasmic CopK protein expressed in Cupriavidus metallidurans CH34 during copper challenge. J Mol Biol 380(2):386–403

    CAS  Google Scholar 

  • Bersch B, Derfoufi KM, De Angelis F, Auquier V, Ekende EN, Mergeay M, Ruysschaert JM, Vandenbussche G (2011) Structural and metal binding characterization of the C-terminal metallochaperone domain of membrane fusion protein SilB from Cupriavidus metallidurans CH34. Biochemistry 50(12):2194–2204

    CAS  Google Scholar 

  • Berven FS, Karlsen OA, Straume AH, Flikka K, Murrell JC, Fjellbirkeland A, Lillehaug JR, Eidhammer I, Jensen HB (2006) Analysing the outer membrane subproteome of Methylococcus capsulatus (Bath) using proteomics and novel biocomputing tools. Arch Microbiol 184(6):362–377

    CAS  Google Scholar 

  • Bloss T, Clemens S, Nies DH (2002) Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta 214(5):783–791

    CAS  Google Scholar 

  • Bolhuis A, Broekhuizen CP, Sorokin A, van Roosmalen ML, Venema G, Bron S, Quax WJ, van Dijl JM (1998) SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem 273(33):21217–21224

    CAS  Google Scholar 

  • Bolla JR, Su CC, Do SV, Radhakrishnan A, Kumar N, Long F, Chou TH, Delmar JA, Lei HT, Rajashankar KR, Shafer WM, Yu EW (2014) Crystal structure of the Neisseria gonorrhoeae MtrD inner membrane multidrug efflux pump. PLoS ONE 9(6):e97903

    Google Scholar 

  • Borges-Walmsley MI, Beauchamp J, Kelly SM, Jumel K, Candlish D, Harding SE, Price NC, Walmsley AR (2003) Identification of oligomerization and drug-binding domains of the membrane fusion protein EmrA. J Biol Chem 278(15):12903–12912

    CAS  Google Scholar 

  • Brown NL, Shih YC, Leang C, Glendinning KJ, Hobman JL, Wilson JR (2002) Mercury transport and resistance. Biochem Soc Trans 30(4):715–718

    CAS  Google Scholar 

  • Bublitz M, Morth JP, Nissen P (2011) P-type ATPases at a glance. J Cell Sci 124(15):2515–2519

    Google Scholar 

  • Chacón KN, Mealman TD, McEvoy MM, Blackburn NJ (2014) Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins. Proc Natl Acad Sci USA 111(43):15373–15378

    Google Scholar 

  • Chan H, Babayan V, Blyumin E, Gandhi C, Hak K, Harake D, Kumar K, Lee P, Li TT, Liu HY, Lo TC, Meyer CJ, Stanford S, Zamora KS, Saier MH Jr (2010) The P-type ATPase superfamily. J Mol Microbiol Biotechnol 19(1–2):5–104

    CAS  Google Scholar 

  • Chao Y, Fu D (2004a) Kinetic study of the antiport mechanism of an Escherichia coli zinc transporter, ZitB. J Biol Chem 279(13):12043–12050

    CAS  Google Scholar 

  • Chao Y, Fu D (2004b) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279(17):17173–17180

    CAS  Google Scholar 

  • Cherezov V, Hofer N, Szebenyi DM, Kolaj O, Wall JG, Gillilan R, Srinivasan V, Jaroniec CP, Caffrey M (2008) Insights into the mode of action of a putative zinc transporter CzrB in Thermus thermophilus. Structure 16(9):1378–1388

    CAS  Google Scholar 

  • Chong LX, Ash MR, Maher MJ, Hinds MG, Xiao ZG, Wedd AG (2009) Unprecedented binding cooperativity between Cu(I) and Cu(II) in the copper resistance protein CopK from Cupriavidus metallidurans CH34: implications from structural studies by NMR spectroscopy and X-Ray crystallography. J Am Chem Soc 131(10):3549–3564

    CAS  Google Scholar 

  • Collard JM, Provoost A, Taghavi S, Mergeay M (1993) A new type of Alcaligenes eutrophus CH34 zinc resistance generated by mutations affecting regulation of the cnr cobalt-nickel resistance system. J Bacteriol 175(3):779–784

    CAS  Google Scholar 

  • Coudray N, Valvo S, Hu M, Lasala R, Kim C, Vink M, Zhou M, Provasi D, Filizola M, Tao J, Fang J, Penczek PA, Ubarretxena-Belandia I, Stokes DL (2013) Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy. Proc Natl Acad Sci USA 110(6):2140–2145

    CAS  Google Scholar 

  • Cubillas C, Vinuesa P, Tabche ML, Garcia-de los Santos A (2013) Phylogenomic analysis of cation diffusion facilitator proteins uncovers Ni2+/Co2+ transporters. Metallomics 5(12):1634–1643

    CAS  Google Scholar 

  • Dame JB, Scarborough GA (1981) Identification of the phosphorylated intermediate of the neurospora plasma-membrane H+-Atpase as beta-aspartyl phosphate. J Biol Chem 256(20):724–730

    Google Scholar 

  • Dang S, Sun L, Huang Y, Lu F, Liu Y, Gong H, Wang J, Yan N (2010) Structure of a fucose transporter in an outward-open conformation. Nature 467(7316):734–738

    CAS  Google Scholar 

  • De Angelis F, Lee JK, O’Connell JD 3rd, Miercke LJ, Verschueren KH, Srinivasan V, Bauvois C, Govaerts C, Robbins RA, Ruysschaert JM, Stroud RM, Vandenbussche G (2010) Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proc Natl Acad Sci USA 107(24):11038–11043

    Google Scholar 

  • de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34(Web Server issue):W362–365

    Google Scholar 

  • Delhaize E, Kataoka T, Hebb DM, White RG, Ryan PR (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15(5):1131–1142

    CAS  Google Scholar 

  • Diaz-Perez C, Cervantes C, Campos-Garcia J, Julian-Sanchez A, Riveros-Rosas H (2007) Phylogenetic analysis of the chromate ion transporter (CHR) superfamily. FEBS J 274(23):6215–6227

    CAS  Google Scholar 

  • Dinh T, Paulsen IT, Saier MH (1994) A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J Bacteriol 176(13):3825–3831

    CAS  Google Scholar 

  • Djoko KY, Xiao Z, Huffman DL, Wedd AG (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(11):4560–4568

    CAS  Google Scholar 

  • Djoko KY, Xiao Z, Wedd AG (2008) Copper resistance in E. coli: the multicopper oxidase PcoA catalyzes oxidation of copper(I) in Cu(I)Cu(II)-PcoC. ChemBioChem 9(10):1579–1582

    CAS  Google Scholar 

  • Doki S, Kato HE, Solcan N, Iwaki M, Koyama M, Hattori M, Iwase N, Tsukazaki T, Sugita Y, Kandori H, Newstead S, Ishitani R, Nureki O (2013) Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc Natl Acad Sci USA 110(28):11343–11348

    CAS  Google Scholar 

  • Dong Q, Mergeay M (1994) Czc/cnr efflux: a three-component chemiosmotic antiport pathway with a 12-transmembrane-helix protein. Mol Microbiol 14(1):185–187

    CAS  Google Scholar 

  • Du D, Wang Z, James NR, Voss JE, Klimont E, Ohene-Agyei T, Venter H, Chiu W, Luisi BF (2014) Structure of the AcrAB-TolC multidrug efflux pump. Nature 509(7501):512–515

    CAS  Google Scholar 

  • Eda S, Maseda H, Nakae T (2003) An elegant means of self-protection in gram-negative bacteria by recognizing and extruding xenobiotics from the periplasmic space. J Biol Chem 278(4):2085–2088

    CAS  Google Scholar 

  • Eicher T, Cha HJ, Seeger MA, Brandstatter L, El-Delik J, Bohnert JA, Kern WV, Verrey F, Grutter MG, Diederichs K, Pos KM (2012) Transport of drugs by the multidrug transporter AcrB involves an access and a deep binding pocket that are separated by a switch-loop. Proc Natl Acad Sci USA 109(15):5687–5692

    CAS  Google Scholar 

  • Eicher T, Seeger MA, Anselmi C, Zhou W, Brandstatter L, Verrey F, Diederichs K, Faraldo-Gomez JD, Pos KM (2014) Coupling of remote alternating-access transport mechanisms for protons and substrates in the multidrug efflux pump AcrB. Elife 3

    Google Scholar 

  • Elkins CA, Nikaido H (2002) Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominantly by two large periplasmic loops. J Bacteriol 184(23):6490–6498

    CAS  Google Scholar 

  • Fang CT, Chen HC, Chuang YP, Chang SC, Wang JT (2002) Cloning of a cation efflux pump gene associated with chlorhexidine resistance in Klebsiella pneumoniae. Antimicrob Agents Chemother 46(6):2024–2028

    CAS  Google Scholar 

  • Federici L, Du D, Walas F, Matsumura H, Fernandez-Recio J, McKeegan KS, Borges-Walmsley MI, Luisi BF, Walmsley AR (2005) The crystal structure of the outer membrane protein VceC from the bacterial pathogen Vibrio cholerae at 1.8 A resolution. J Biol Chem 280(15):15307–15314

    Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(Database issue):D222–230

    Google Scholar 

  • Franke S, Grass G, Nies DH (2001) The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147(Pt 4):965–972

    Google Scholar 

  • Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185(13):3804–3812

    Google Scholar 

  • Fujihira E, Tamura N, Yamaguchi A (2002) Membrane topology of a multidrug efflux transporter, AcrB, in Escherichia coli. J Biochem 131(1):145–151

    CAS  Google Scholar 

  • Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14(3–4):251–270

    CAS  Google Scholar 

  • Garcia-Dominguez M, Lopez-Maury L, Florencio FJ, Reyes JC (2000) A gene cluster involved in metal homeostasis in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182(6):1507–1514

    CAS  Google Scholar 

  • Goldberg M, Pribyl T, Juhnke S, Nies DH (1999) Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J Biol Chem 274(37):26065–26070

    CAS  Google Scholar 

  • Gonzalez-Guerrero M, Arguello JM (2008) Mechanism of Cu+-transporting ATPases: soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites. Proc Natl Acad Sci USA 105(16):5992–5997

    CAS  Google Scholar 

  • Gonzalez-Guerrero M, Eren E, Rawat S, Stemmler TL, Arguello JM (2008) Structure of the two transmembrane Cu+ transport sites of the Cu+-ATPases. J Biol Chem 283(44):29753–29759

    CAS  Google Scholar 

  • Gonzalez-Guerrero M, Hong D, Arguello JM (2009) Chaperone-mediated Cu+ delivery to Cu+ transport ATPases: requirement of nucleotide binding. J Biol Chem 284(31):20804–20811

    CAS  Google Scholar 

  • Gotoh N, Kusumi T, Tsujimoto H, Wada T, Nishino T (1999) Topological analysis of an RND family transporter. MexD of Pseudomonas aeruginosa. FEBS Lett 458(1):32–36

    CAS  Google Scholar 

  • Gourdon P, Liu XY, Skjorringe T, Morth JP, Moller LB, Pedersen BP, Nissen P (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475(7354):59–64

    CAS  Google Scholar 

  • Grass G, Grosse C, Nies DH (2000) Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J Bacteriol 182(5):1390–1398

    CAS  Google Scholar 

  • Grass G, Fan B, Rosen BP, Lemke K, Schlegel HG, Rensing C (2001) NreB from Achromobacter xylosoxidans 31A Is a nickel-induced transporter conferring nickel resistance. J Bacteriol 183(9):2803–2807

    CAS  Google Scholar 

  • Grass G, Fricke B, Nies DH (2005a) Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals 18(4):437–448

    CAS  Google Scholar 

  • Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005b) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183(1):9–18

    CAS  Google Scholar 

  • Greene NP, Hinchliffe P, Crow A, Ababou A, Hughes C, Koronakis V (2013) Structure of an atypical periplasmic adaptor from a multidrug efflux pump of the spirochete Borrelia burgdorferi. FEBS Lett 587(18):2984–2988

    CAS  Google Scholar 

  • Griffith JK, Baker ME, Rouch DA, Page MG, Skurray RA, Paulsen IT, Chater KF, Baldwin SA, Henderson PJ (1992) Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol 4(4):684–695

    CAS  Google Scholar 

  • Grosse C, Grass G, Anton A, Franke S, Santos AN, Lawley B, Brown NL, Nies DH (1999) Transcriptional organization of the czc heavy-metal homeostasis determinant from Alcaligenes eutrophus. J Bacteriol 181(8):2385–2393

    CAS  Google Scholar 

  • Grosse C, Anton A, Hoffmann T, Franke S, Schleuder G, Nies DH (2004) Identification of a regulatory pathway that controls the heavy-metal resistance system Czc via promoter czcNp in Ralstonia metallidurans. Arch Microbiol 182(2–3):109–118

    CAS  Google Scholar 

  • Guan L, Ehrmann M, Yoneyama H, Nakae T (1999) Membrane topology of the xenobiotic-exporting subunit, MexB, of the MexA, B-OprM extrusion pump in Pseudomonas aeruginosa. J Biol Chem 274(15):10517–10522

    CAS  Google Scholar 

  • Guffanti AA, Wei Y, Rood SV, Krulwich TA (2002) An antiport mechanism for a member of the cation diffusion facilitator family: divalent cations efflux in exchange for K+ and H+. Mol Microbiol 45(1):145–153

    CAS  Google Scholar 

  • Hamlett NV, Landale EC, Davis BH, Summers AO (1992) Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding. J Bacteriol 174(20):6377–6385

    CAS  Google Scholar 

  • Haney CJ, Grass G, Franke S, Rensing C (2005) New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol 32(6):215–226

    CAS  Google Scholar 

  • Harley KT, Saier MH (2000) A novel ubiquitous family of putative efflux transporters. J Mol Microbiol Biotechnol 2(2):195–198

    CAS  Google Scholar 

  • Hatori Y, Majima E, Tsuda T, Toyoshima C (2007) Domain organization and movements in heavy metal ion pumps: papain digestion of CopA, a Cu+-transporting ATPase. J Biol Chem 282(35):25213–25221

    CAS  Google Scholar 

  • Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110

    CAS  Google Scholar 

  • Higgins MK, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Structure of the periplasmic component of a bacterial drug efflux pump. Proc Natl Acad Sci USA 101(27):9994–9999

    CAS  Google Scholar 

  • Higuchi T, Hattori M, Tanaka Y, Ishitani R, Nureki O (2009) Crystal structure of the cytosolic domain of the cation diffusion facilitator family protein. Proteins Struct Func Bioinform 76(3):768–771

    CAS  Google Scholar 

  • Hinchliffe P, Greene NP, Paterson NG, Crow A, Hughes C, Koronakis V (2014) Structure of the periplasmic adaptor protein from a major facilitator superfamily (MFS) multidrug efflux pump. FEBS Lett 588(17):3147–3153

    CAS  Google Scholar 

  • Hirai T, Subramaniam S (2004) Structure and transport mechanism of the bacterial oxalate transporter OxlT. Biophys J 87(5):3600–3607

    CAS  Google Scholar 

  • Hlozkova K, Suman J, Strnad H, Ruml T, Paces V, Kotrba P (2013) Characterization of pbt genes conferring increased Pb2+ and Cd2+ tolerance upon Achromobacter xylosoxidans A8. Res Microbiol 164(10):1009–1018

    CAS  Google Scholar 

  • Hoch E, Lin W, Chai J, Hershfinkel M, Fu D, Sekler I (2012) Histidine pairing at the metal transport site of mammalian ZnT transporters controls Zn2+ over Cd2+ selectivity. Proc Natl Acad Sci USA 109(19):7202–7207

    CAS  Google Scholar 

  • Huang L, Tepaamorndech S (2013) The SLC30 family of zinc transporters—a review of current understanding of their biological and pathophysiological roles. Mol Aspects Med 34(2–3):548–560

    CAS  Google Scholar 

  • Husain F, Nikaido H (2010) Substrate path in the AcrB multidrug efflux pump of Escherichia coli. Mol Microbiol 78(2):320–330

    CAS  Google Scholar 

  • Husain F, Bikhchandani M, Nikaido H (2011) Vestibules are part of the substrate path in the multidrug efflux transporter AcrB of Escherichia coli. J Bacteriol 193(20):5847–5849

    CAS  Google Scholar 

  • Hvorup RN, Saier MH (2002) Sequence similarity between the channel-forming domains of voltage-gated ion channel proteins and the C-terminal domains of secondary carriers of the major facilitator superfamily. Microbiol Sgm 148(Pt 12):3760–3762

    CAS  Google Scholar 

  • Jack DL, Yang NM, Saier MH Jr (2001) The drug/metabolite transporter superfamily. Eur J Biochem 268(13):3620–3639

    CAS  Google Scholar 

  • Janganan TK, Bavro VN, Zhang L, Matak-Vinkovic D, Barrera NP, Venien-Bryan C, Robinson CV, Borges-Walmsley MI, Walmsley AR (2011) Evidence for the assembly of a bacterial tripartite multidrug pump with a stoichiometry of 3:6:3. J Biol Chem 286(30):26900–26912

    CAS  Google Scholar 

  • Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Médigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M (2010) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS ONE 5(5):e10433

    Google Scholar 

  • Jessen-Marshall AE, Paul NJ, Brooker RJ (1995) The conserved motif, GXXX(D/E)(R/K)XG[X](R/K)(R/K), in hydrophilic loop 2/3 of the lactose permease. J Biol Chem 270(27):16251–16257

    CAS  Google Scholar 

  • Jessen-Marshall AE, Parker NJ, Brooker RJ (1997) Suppressor analysis of mutations in the loop 2-3 motif of lactose permease: evidence that glycine-64 is an important residue for conformational changes. J Bacteriol 179(8):2616–2622

    CAS  Google Scholar 

  • Jia S, Wang Z, Zhang XX, Liu B, Li W, Cheng S (2013) Metagenomic analysis of cadmium and copper resistance genes in activated sludge of a tannery wastewater treatment plant. J Environ Biol 34(2 Spec No):375–380

    Google Scholar 

  • Johnson JM, Church GM (1999) Alignment and structure prediction of divergent protein families: periplasmic and outer membrane proteins of bacterial efflux pumps. J Mol Biol 287(3):695–715

    CAS  Google Scholar 

  • Johs A, Harwood IM, Parks JM, Nauss RE, Smith JC, Liang L, Miller SM (2011) Structural characterization of intramolecular Hg(2+) transfer between flexibly linked domains of mercuric ion reductase. J Mol Biol 413(3):639–656

    CAS  Google Scholar 

  • Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240

    CAS  Google Scholar 

  • Juhnke S, Peitzsch N, Hubener N, Grosse C, Nies DH (2002) New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch Microbiol 179(1):15–25

    CAS  Google Scholar 

  • Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A (2003) Prediction of lipoprotein signal peptides in gram-negative bacteria. Protein Sci 12(8):1652–1662

    CAS  Google Scholar 

  • Kambe T (2012) Molecular architecture and function of ZnT transporters. Curr Top Membr 69:199–220

    CAS  Google Scholar 

  • Kambe T, Narita H, Yamaguchi-Iwai Y, Hirose J, Amano T, Sugiura N, Sasaki R, Mori K, Iwanaga T, Nagao M (2002) Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic beta cells. J Biol Chem 277(21):19049–19055

    CAS  Google Scholar 

  • Kamizono A, Nishizawa M, Teranishi Y, Murata K, Kimura A (1989) Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol Gen Genet 219(1–2):161–167

    CAS  Google Scholar 

  • Kawachi M, Kobae Y, Mimura T, Maeshima M (2008) Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn(2+)/H(+) antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283(13):8374–8383

    CAS  Google Scholar 

  • Kim HS, Nagore D, Nikaido H (2010) Multidrug efflux pump MdtBC of Escherichia coli is active only as a B2C heterotrimer. J Bacteriol 192(5):1377–1386

    CAS  Google Scholar 

  • Kim EH, Nies DH, McEvoy MM, Rensing C (2011) Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 193(10):2381–2387

    CAS  Google Scholar 

  • Kim JS, Jeong H, Song S, Kim HY, Lee K, Hyun J, Ha NC (2015) Structure of the tripartite multidrug efflux pump AcrAB-TolC suggests an alternative assembly mode. Mol Cells 38(2):180–186

    Google Scholar 

  • Kiyono M, Sone Y, Nakamura R, Pan-Hou H, Sakabe K (2009) The MerE protein encoded by transposon Tn21 is a broad mercury transporter in Escherichia coli. FEBS Lett 583(7):1127–1131

    CAS  Google Scholar 

  • Koronakis V, Li J, Koronakis E, Stauffer K (1997) Structure of TolC, the outer membrane component of the bacterial type I efflux system, derived from two-dimensional crystals. Mol Microbiol 23(3):617–626

    CAS  Google Scholar 

  • Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405(6789):914–919

    CAS  Google Scholar 

  • Koronakis V, Eswaran J, Hughes C (2004) Structure and function of TolC: the bacterial exit duct for proteins and drugs. Annu Rev Biochem 73:467–489

    CAS  Google Scholar 

  • Kuhlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5(4):282–295

    Google Scholar 

  • Kulathila R, Kulathila R, Indic M, van den Berg B (2011) Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. PLoS ONE 6(1):e15610

    CAS  Google Scholar 

  • Laitaoja M, Valjakka J, Janis J (2013) Zinc coordination spheres in protein structures. Inorg Chem 52(19):10983–10991

    CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948

    CAS  Google Scholar 

  • Law CJ, Maloney PC, Wang DN (2008) Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 62:289–305

    CAS  Google Scholar 

  • Ledwidge R, Patel B, Dong A, Fiedler D, Falkowski M, Zelikova J, Summers AO, Pai EF, Miller SM (2005) NmerA, the metal binding domain of mercuric ion reductase, removes Hg2+ from proteins, delivers it to the catalytic core, and protects cells under glutathione-depleted conditions. Biochemistry 44(34):11402–11416

    CAS  Google Scholar 

  • Ledwidge R, Hong B, Dotsch V, Miller SM (2010) NmerA of Tn501 mercuric ion reductase: structural modulation of the pKa values of the metal binding cysteine thiols. Biochemistry 49(41):8988–8998

    CAS  Google Scholar 

  • Lee SM, Grass G, Haney CJ, Fan B, Rosen BP, Anton A, Nies DH, Rensing C (2002) Functional analysis of the Escherichia coli zinc transporter ZitB. FEMS Microbiol Lett 215(2):273–278

    CAS  Google Scholar 

  • Lei HT, Bolla JR, Bishop NR, Su CC, Yu EW (2014a) Crystal structures of CusC review conformational changes accompanying folding and transmembrane channel formation. J Mol Biol 426(2):403–411

    CAS  Google Scholar 

  • Lei HT, Chou TH, Su CC, Bolla JR, Kumar N, Radhakrishnan A, Long F, Delmar JA, Do SV, Rajashankar KR, Shafer WM, Yu EW (2014b) Crystal structure of the open state of the Neisseria gonorrhoeae MtrE outer membrane channel. PLoS ONE 9(6):e97475

    Google Scholar 

  • Li L, Kaplan J (2001) The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J Biol Chem 276(7):5036–5043

    CAS  Google Scholar 

  • Lian P, Guo HB, Riccardi D, Dong A, Parks JM, Xu Q, Pai EF, Miller SM, Wei DQ, Smith JC, Guo H (2014) X-ray structure of a Hg2+ complex of mercuric reductase (MerA) and quantum mechanical/molecular mechanical study of Hg2+ transfer between the C-terminal and buried catalytic site cysteine pairs. Biochemistry 53(46):7211–7222

    CAS  Google Scholar 

  • Liesegang H, Lemke K, Siddiqui RA, Schlegel HG (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175(3):767–778

    CAS  Google Scholar 

  • Lobedanz S, Bokma E, Symmons MF, Koronakis E, Hughes C, Koronakis V (2007) A periplasmic coiled-coil interface underlying TolC recruitment and the assembly of bacterial drug efflux pumps. Proc Natl Acad Sci USA 104(11):4612–4617

    CAS  Google Scholar 

  • Loftin IR, Franke S, Roberts SA, Weichsel A, Heroux A, Montfort WR, Rensing C, McEvoy MM (2005) A novel copper-binding fold for the periplasmic copper resistance protein CusF. Biochemistry 44(31):10533–10540

    CAS  Google Scholar 

  • Loftin IR, Franke S, Blackburn NJ, McEvoy MM (2007) Unusual Cu(I)/Ag(I) coordination of Escherichia coli CusF as revealed by atomic resolution crystallography and X-ray absorption spectroscopy. Protein Sci 16(10):2287–2293

    CAS  Google Scholar 

  • Loftin IR, Blackburn NJ, McEvoy MM (2009) Tryptophan Cu(I)-pi interaction fine-tunes the metal binding properties of the bacterial metallochaperone CusF. J Biol Inorg Chem 14(6):905–912

    CAS  Google Scholar 

  • Lonetto M, Gribskov M, Gross CA (1992) The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174(12):3843–3849

    CAS  Google Scholar 

  • Lonetto MA, Brown KL, Rudd KE, Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci USA 91(16):7573–7577

    CAS  Google Scholar 

  • Long F, Su CC, Zimmermann MT, Boyken SE, Rajashankar KR, Jernigan RL, Yu EW (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467(7314):484–488

    CAS  Google Scholar 

  • Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317(5845):1746–1748

    CAS  Google Scholar 

  • Lu S, Zgurskaya HI (2013) MacA, a periplasmic membrane fusion protein of the macrolide transporter MacAB-TolC, binds lipopolysaccharide core specifically and with high affinity. J Bacteriol 195(21):4865–4872

    CAS  Google Scholar 

  • Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat Struct Mol Biol 16(10):1063–1067

    CAS  Google Scholar 

  • Lund PA, Brown NL (1987) Role of the merT and merP gene products of transposon Tn501 in the induction and expression of resistance to mercuric ions. Gene 52(2–3):207–214

    CAS  Google Scholar 

  • Lycklama ANJA, Driessen AJ (2012) The bacterial Sec-translocase: structure and mechanism. Philos Trans R Soc Lond B Biol Sci 367(1592):1016–1028

    Google Scholar 

  • MacDiarmid CW, Milanick MA, Eide DJ (2002) Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae. J Biol Chem 277(42):39187–39194

    CAS  Google Scholar 

  • Maiden MC, Davis EO, Baldwin SA, Moore DC, Henderson PJ (1987) Mammalian and bacterial sugar transport proteins are homologous. Nature 325(6105):641–643

    CAS  Google Scholar 

  • Maillard AP, Girard E, Ziani W, Petit-Hartlein I, Kahn R, Covès J (2014) The crystal structure of the anti-sigma factor CnrY in complex with the sigma factor CnrH shows a new structural class of anti-sigma factors targeting extracytoplasmic function sigma factors. J Mol Biol 426(12):2313–2327

    Google Scholar 

  • Maillard AP, Künnemann S, Grosse C, Volbeda A, Schleuder G, Petit-Härtlein I, de Rosny E, Nies DH, Covès J (2015) Response of CnrX from Cupriavidus metallidurans CH34 to nickel binding. Metallomics 7(4):622–631

    Google Scholar 

  • Mandal AK, Yang Y, Kertesz TM, Arguello JM (2004) Identification of the transmembrane metal binding site in Cu+-transporting PIB-type ATPases. J Biol Chem 279(52):54802–54807

    CAS  Google Scholar 

  • Maret W (2012) New perspectives of zinc coordination environments in proteins. J Inorg Biochem 111:110–116

    CAS  Google Scholar 

  • Marger MD, Saier MH (1993) A major superfamily of transmembrane facilitators that catalyze uniport, Symport and Antiport. Trends Biochem Sci 18(1):13–20

    CAS  Google Scholar 

  • Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann a, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim Sa, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126(4):1646–1667

    Google Scholar 

  • Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27(2–3):385–410

    CAS  Google Scholar 

  • Mijnendonckx K, Provoost A, Monsieurs P, Leys N, Mergeay M, Mahillon J, Van Houdt R (2011) Insertion sequence elements in Cupriavidus metallidurans CH34: distribution and role in adaptation. Plasmid 65(3):193–203

    CAS  Google Scholar 

  • Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P (2006) Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14(3):577–587

    CAS  Google Scholar 

  • Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43(Database issue):D213–221

    Google Scholar 

  • Mok T, Chen JS, Shlykov MA, Saier MH (2012) Bioinformatic analyses of bacterial mercury ion (Hg2+) Transporters. Water Air Soil Pollut 223(7):4443–4457

    CAS  Google Scholar 

  • Monchy S, Benotmane MA, Wattiez R, van Aelst S, Auquier V, Borremans B, Mergeay M, Taghavi S, van der Lelie D, Vallaeys T (2006a) Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152(Pt 6):1765–1776

    CAS  Google Scholar 

  • Monchy S, Vallaeys T, Bossus A, Mergeay M (2006b) Metal transport ATPase genes from Cupriavidus metallidurans CH34: a transcriptomic approach. Int J Environ Anal Chem 86(9):677–692

    CAS  Google Scholar 

  • Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, van der Lelie D, Mergeay M (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 189(20):7417–7425

    CAS  Google Scholar 

  • Monsieurs P, Moors H, Van Houdt R, Janssen PJ, Janssen A, Coninx I, Mergeay M, Leys N (2011) Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network. Biometals 24(6):1133–1151

    CAS  Google Scholar 

  • Monsieurs P, Provoost A, Mijnendonckx K, Leys N, Gaudreau C, Van Houdt R (2013) Genome sequence of Cupriavidus metallidurans Strain H1130, isolated from an invasive human infection. Genome Announcements 1(6):e01013–e01051

    Google Scholar 

  • Monsieurs P, Mijnendonckx K, Provoost A, Venkateswaran K, Ott CM, Leys N, Van Houdt R (2014) Genome sequences of Cupriavidus metallidurans strains NA1, NA4, and NE12, isolated from space equipment. Genome Announc 2(4):e00714–e00719

    Google Scholar 

  • Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genom 8:107

    Google Scholar 

  • Moore MJ, Walsh CT (1989) Mutagenesis of the N- and C-terminal cysteine pairs of Tn501 mercuric ion reductase: consequences for bacterial detoxification of mercurials. Biochemistry 28(3):1183–1194

    CAS  Google Scholar 

  • Morby AP, Hobman JL, Brown NL (1995) The role of cysteine residues in the transport of mercuric ions by the Tn501 MerT and MerP mercury-resistance proteins. Mol Microbiol 17(1):25–35

    CAS  Google Scholar 

  • Munkelt D, Grass G, Nies DH (2004) The chromosomally encoded cation diffusion facilitator proteins DmeF and FieF from Wautersia metallidurans CH34 are transporters of broad metal specificity. J Bacteriol 186(23):8036–8043

    CAS  Google Scholar 

  • Murakami S, Nakashima R, Yamashita E, Yamaguchi A (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419(6907):587–593

    CAS  Google Scholar 

  • Murakami S, Nakashima R, Yamashita E, Matsumoto T, Yamaguchi A (2006) Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443(7108):173–179

    CAS  Google Scholar 

  • Murgia C, Vespignani I, Cerase J, Nobili F, Perozzi G (1999) Cloning, expression, and vesicular localization of zinc transporter Dri 27/ZnT4 in intestinal tissue and cells. Am J Physiol 277(6 Pt 1):G1231–G1239

    CAS  Google Scholar 

  • Murzin AG (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J 12(3):861–867

    CAS  Google Scholar 

  • Nakajima A, Sugimoto Y, Yoneyama H, Nakae T (2000) Localization of the outer membrane subunit OprM of resistance-nodulation-cell division family multicomponent efflux pump in Pseudomonas aeruginosa. J Biol Chem 275(39):30064–30068

    CAS  Google Scholar 

  • Nakashima R, Sakurai K, Yamasaki S, Nishino K, Yamaguchi A (2011) Structures of the multidrug exporter AcrB reveal a proximal multisite drug-binding pocket. Nature 480(7378):565–569

    CAS  Google Scholar 

  • Ngonlong Ekendé EC (2012) Towards a better understanding of bacterial resistance to heavy metal ions: the case of the Sil and Zne systems from Cupriavidus metallidurans CH34. Université Libre de Bruxelles, Brussels

    Google Scholar 

  • Nies DH (1992) CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc, and cadmium (czc system) in Alcaligenes eutrophus. J Bacteriol 174(24):8102–8110

    CAS  Google Scholar 

  • Nies DH (1995) The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177(10):2707–2712

    CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2–3):313–339

    CAS  Google Scholar 

  • Nies DH (2013) RND efflux pumps for metal cations. In: Yu EW, Zhang Q, Brown MH (eds) Microbial efflux pumps. Caister Academic Press, Norfolk

    Google Scholar 

  • Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14(2):186–199

    CAS  Google Scholar 

  • Nies D, Mergeay M, Friedrich B, Schlegel HG (1987) Cloning of plasmid genes encoding resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus CH34. J Bacteriol 169(10):4865–4868

    CAS  Google Scholar 

  • Nies DH, Nies A, Chu L, Silver S (1989) Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus. Proc Natl Acad Sci USA 86(19):7351–7355

    CAS  Google Scholar 

  • Nies A, Nies DH, Silver S (1990) Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J Biol Chem 265(10):5648–5653

    CAS  Google Scholar 

  • Nies DH, Koch S, Wachi S, Peitzsch N, Saier MH Jr (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180(21):5799–5802

    CAS  Google Scholar 

  • Nies DH, Rehbein G, Hoffmann T, Baumann C, Grosse C (2006) Paralogs of genes encoding metal resistance proteins in Cupriavidus metallidurans strain CH34. J Mol Microbiol Biotechnol 11(1–2):82–93

    CAS  Google Scholar 

  • Nikaido H, Pages JM (2012) Broad-specificity efflux pumps and their role in multidrug resistance of gram-negative bacteria. FEMS Microbiol Rev 36(2):340–363

    CAS  Google Scholar 

  • Ohana E, Hoch E, Keasar C, Kambe T, Yifrach O, Hershfinkel M, Sekler I (2009) Identification of the Zn2+ binding site and mode of operation of a mammalian Zn2+ transporter. J Biol Chem 284(26):17677–17686

    CAS  Google Scholar 

  • Ohene-Agyei T, Lea JD, Venter H (2012) Mutations in MexB that affect the efflux of antibiotics with cytoplasmic targets. FEMS Microbiol Lett 333(1):20–27

    CAS  Google Scholar 

  • Okkeri J, Haltia T (2006) The metal-binding sites of the zinc-transporting P-type ATPase of Escherichia coli. Lys693 and Asp714 in the seventh and eighth transmembrane segments of ZntA contribute to the coupling of metal binding and ATPase activity. Biochim Biophys Acta 1757(11):1485–1495

    CAS  Google Scholar 

  • Olsson-Francis K, Van Houdt R, Mergeay M, Leys N, Cockell CS (2010) Microarray analysis of a microbe-mineral interaction. Geobiology 8(5):446–456

    CAS  Google Scholar 

  • Opella SJ, DeSilva TM, Veglia G (2002) Structural biology of metal-binding sequences. Curr Opin Chem Biol 6(2):217–223

    CAS  Google Scholar 

  • Padilla-Benavides T, George Thompson AM, McEvoy MM, Arguello JM (2014) Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J Biol Chem 289(30):20492–20501

    CAS  Google Scholar 

  • Pak JE, Ekende EN, Kifle EG, O’Connell JD 3rd, De Angelis F, Tessema MB, Derfoufi KM, Robles-Colmenares Y, Robbins RA, Goormaghtigh E, Vandenbussche G, Stroud RM (2013) Structures of intermediate transport states of ZneA, a Zn(II)/proton antiporter. Proc Natl Acad Sci USA 110(46):18484–18489

    CAS  Google Scholar 

  • Palmgren MG, Nissen P (2011) P-type ATPases. Annu Rev Biophys 40:243–266

    CAS  Google Scholar 

  • Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62(1):1–34

    CAS  Google Scholar 

  • Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507(7490):68–72

    CAS  Google Scholar 

  • Patel K, Kumar A, Durani S (2007) Analysis of the structural consensus of the zinc coordination centers of metalloprotein structures. Biochim Biophys Acta 1774(10):1247–1253

    CAS  Google Scholar 

  • Paulsen IT, Saier MH Jr (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156(2):99–103

    CAS  Google Scholar 

  • Paulsen IT, Brown MH, Skurray RA (1996) Proton-dependent multidrug efflux systems. Microbiol Rev 60(4):575–608

    CAS  Google Scholar 

  • Paulsen IT, Park JH, Choi PS, Saier MH (1997) A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Lett 156(1):1–8

    CAS  Google Scholar 

  • Pei XY, Hinchliffe P, Symmons MF, Koronakis E, Benz R, Hughes C, Koronakis V (2011) Structures of sequential open states in a symmetrical opening transition of the TolC exit duct. Proc Natl Acad Sci USA 108(5):2112–2117

    CAS  Google Scholar 

  • Perron K, Caille O, Rossier C, Van Delden C, Dumas JL, Kohler T (2004) CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279(10):8761–8768

    CAS  Google Scholar 

  • Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98(17):9995–10000

    CAS  Google Scholar 

  • Petit-Haertlein I, Girard E, Sarret G, Hazemann JL, Gourhant P, Kahn R, Covès J (2010) Evidence for conformational changes upon copper binding to Cupriavidus metallidurans CzcE. Biochemistry 49(9):1913–1922

    CAS  Google Scholar 

  • Pimentel BE, Moreno-Sanchez R, Cervantes C (2002) Efflux of chromate by Pseudomonas aeruginosa cells expressing the ChrA protein. FEMS Microbiol Lett 212(2):249–254

    CAS  Google Scholar 

  • Pompidor G, Zoropogui A, Kahn R, Covès J (2007) Overproduction, purification and preliminary X-ray diffraction analysis of CzcE from Cupriavidus metallidurans CH34. Acta Crystallogr Sect F: Struct Biol Cryst Commun 63:884–886

    Google Scholar 

  • Pompidor G, Maillard AP, Girard E, Gambarelli S, Kahn R, Covès J (2008) X-ray structure of the metal-sensor CnrX in both the apo- and copper-bound forms. FEBS Lett 582(28):3954–3958

    Google Scholar 

  • Pompidor G, Girard E, Maillard A, Ramella-Pairin S, Bersch B, Kahn R, Covès J (2009) Biostructural analysis of the metal-sensor domain of CnrX from Cupriavidus metallidurans CH34. Anton Leeuw Int J G 96(2):141–148

    Google Scholar 

  • Poole K, Krebes K, McNally C, Neshat S (1993) Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J Bacteriol 175(22):7363–7372

    CAS  Google Scholar 

  • Pos KM (2009) Drug transport mechanism of the AcrB efflux pump. Biochim Biophys Acta 1794(5):782–793

    CAS  Google Scholar 

  • Post RL, Jolly PC (1957) The linkage of sodium, potassium, and ammonium active transport across the human erythrocyte membrane. Biochim Biophys Acta 25(1):118–128

    CAS  Google Scholar 

  • Post RL, Kume S, Tobin T, Orcutt B, Sen AK (1969) Flexibility of an active center in sodium-plus-potassium adenosine triphosphatase. J Gen Physiol 54(1):306–326

    CAS  Google Scholar 

  • Powlowski J, Sahlman L (1999) Reactivity of the two essential cysteine residues of the periplasmic mercuric ion-binding protein. MerP. J Biol Chem 274(47):33320–33326

    CAS  Google Scholar 

  • Radestock S, Forrest LR (2011) The alternating-access mechanism of MFS transporters arises from inverted-topology repeats. J Mol Biol 407(5):698–715

    CAS  Google Scholar 

  • Rahman M, Patching SG, Ismat F, Henderson PJ, Herbert RB, Baldwin SA, McPherson MJ (2008) Probing metal ion substrate-binding to the E. coli ZitB exporter in native membranes by solid state NMR. Mol Membr Biol 25(8):683–690

    CAS  Google Scholar 

  • Ramirez-Diaz MI, Diaz-Perez C, Vargas E, Riveros-Rosas H, Campos-Garcia J, Cervantes C (2008) Mechanisms of bacterial resistance to chromium compounds. Biometals 21(3):321–332

    CAS  Google Scholar 

  • Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH Jr (2012) The major facilitator superfamily (MFS) revisited. FEBS J 279(11):2022–2035

    CAS  Google Scholar 

  • Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27(2–3):197–213

    CAS  Google Scholar 

  • Rensing C, Pribyl T, Nies DH (1997) New functions for the three subunits of the CzcCBA cation-proton antiporter. J Bacteriol 179(22):6871–6879

    CAS  Google Scholar 

  • Rensing C, Ghosh M, Rosen BP (1999) Families of soft-metal-ion-transporting ATPases. J Bacteriol 181(19):5891–5897

    CAS  Google Scholar 

  • Rosenzweig AC, Huffman DL, Hou MY, Wernimont AK, Pufahl RA, O’Halloran TV (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 A resolution. Structure 7(6):605–617

    CAS  Google Scholar 

  • Rubin RA, Levy SB, Heinrikson RL, Kezdy FJ (1990) Gene duplication in the evolution of the two complementing domains of gram-negative bacterial tetracycline efflux proteins. Gene 87(1):7–13

    CAS  Google Scholar 

  • Ruggerone P, Murakami S, Pos KM, Vargiu AV (2013) RND efflux pumps: structural information translated into function and inhibition mechanisms. Curr Top Med Chem 13(24):3079–3100

    CAS  Google Scholar 

  • Sahlman L, Jonsson BH (1992) Purification and properties of the mercuric-ion-binding protein MerP. Eur J Biochem 205(1):375–381

    CAS  Google Scholar 

  • Sahlman L, Skarfstad EG (1993) Mercuric ion binding abilities of MerP variants containing only one cysteine. Biochem Biophys Res Commun 196(2):583–588

    CAS  Google Scholar 

  • Saier MH Jr, Reddy VS, Tamang DG, Vastermark A (2014) The transporter classification database. Nucleic Acids Res 42(Database issue):D251–258

    Google Scholar 

  • Saier MH Jr, Tam R, Reizer A, Reizer J (1994) Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11(5):841–847

    CAS  Google Scholar 

  • Saier MH Jr, Paulsen IT, Sliwinski MK, Pao SS, Skurray RA, Nikaido H (1998) Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J 12(3):265–274

    CAS  Google Scholar 

  • Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1(2):257–279

    CAS  Google Scholar 

  • Saier MH, Goldman SR, Maile RR, Moreno MS, Weyler W, Yang N, Paulsen IT (2002) Transport capabilities encoded within the Bacillus subtilis genome. J Mol Microbiol Biotechnol 4(1):37–67

    CAS  Google Scholar 

  • Sarret G, Favier A, Covès J, Hazemann JL, Mergeay M, Bersch B (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(11):3770–3777

    Google Scholar 

  • Sazinsky MH, LeMoine B, Orofino M, Davydov R, Bencze KZ, Stemmler TL, Hoffman BM, Arguello JM, Rosenzweig AC (2007) Characterization and structure of a Zn2+ and [2Fe-2S]-containing copper chaperone from Archaeoglobus fulgidus. J Biol Chem 282(35):25950–25959

    CAS  Google Scholar 

  • Scherer J, Nies DH (2009) CzcP is a novel efflux system contributing to transition metal resistance in Cupriavidus metallidurans CH34. Mol Microbiol 73(4):601–621

    CAS  Google Scholar 

  • Seeger MA, Schiefner A, Eicher T, Verrey F, Diederichs K, Pos KM (2006) Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313(5791):1295–1298

    CAS  Google Scholar 

  • Seeger MA, von Ballmoos C, Eicher T, Brandstatter L, Verrey F, Diederichs K, Pos KM (2008) Engineered disulfide bonds support the functional rotation mechanism of multidrug efflux pump AcrB. Nat Struct Mol Biol 15(2):199–205

    CAS  Google Scholar 

  • Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3(December):399

    Google Scholar 

  • Sendra V, Cannella D, Bersch B, Fieschi F, Menage S, Lascoux D, Covès J (2006) CopH from Cupriavidus metallidurans CH34. A novel periplasmic copper-binding protein. Biochemistry 45(17):5557–5566

    Google Scholar 

  • Sendra V, Gambarelli S, Bersch B, Covès J (2009) Site-directed mutagenesis reveals a conservation of the copper-binding site and the crucial role of His24 in CopH from Cupriavidus metallidurans CH34. J Inorg Biochem 103(12):1721–1728

    Google Scholar 

  • Sennhauser G, Amstutz P, Briand C, Storchenegger O, Grutter MG (2007) Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol 5(1):e7

    Google Scholar 

  • Sennhauser G, Bukowska MA, Briand C, Grutter MG (2009) Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa. J Mol Biol 389(1):134–145

    CAS  Google Scholar 

  • Serre L, Rossy E, Pebay-Peyroula E, Cohen-Addad C, Covès J (2004) Crystal structure of the oxidized form of the periplasmic mercury-binding protein MerP from Ralstonia metallidurans CH34. J Mol Biol 339(1):161–171

    Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789

    CAS  Google Scholar 

  • Solcan N, Kwok J, Fowler PW, Cameron AD, Drew D, Iwata S, Newstead S (2012) Alternating access mechanism in the POT family of oligopeptide transporters. EMBO J 31(16):3411–3421

    CAS  Google Scholar 

  • Solioz M, Vulpe C (1996) CPx-type ATPases: A class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21(7):237–241

    CAS  Google Scholar 

  • Sone Y, Nakamura R, Pan-Hou H, Itoh T, Kiyono M (2013) Role of MerC, MerE, MerF, MerT, and/or MerP in resistance to mercurials and the transport of mercurials in Escherichia coli. Biol Pharm Bull 36(11):1835–1841

    CAS  Google Scholar 

  • Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6:175–182

    CAS  Google Scholar 

  • Steele RA, Opella SJ (1997) Structures of the reduced and mercury-bound forms of MerP, the periplasmic protein from the bacterial mercury detoxification system. Biochemistry 36(23):6885–6895

    CAS  Google Scholar 

  • Su CC, Yang F, Long F, Reyon D, Routh MD, Kuo DW, Mokhtari AK, Van Ornam JD, Rabe KL, Hoy JA, Lee YJ, Rajashankar KR, Yu EW (2009) Crystal structure of the membrane fusion protein CusB from Escherichia coli. J Mol Biol 393(2):342–355

    CAS  Google Scholar 

  • Su CC, Long F, Zimmermann MT, Rajashankar KR, Jernigan RL, Yu EW (2011) Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 470(7335):558–562

    CAS  Google Scholar 

  • Su CC, Long F, Lei HT, Bolla JR, Do SV, Rajashankar KR, Yu EW (2012) Charged amino acids (R83, E567, D617, E625, R669, and K678) of CusA are required for metal ion transport in the Cus efflux system. J Mol Biol 422(3):429–441

    CAS  Google Scholar 

  • Su CC, Radhakrishnan A, Kumar N, Long F, Bolla JR, Lei HT, Delmar JA, Do SV, Chou TH, Rajashankar KR, Zhang Q, Yu EW (2014) Crystal structure of the Campylobacter jejuni CmeC outer membrane channel. Protein Sci 23(7):954–961

    CAS  Google Scholar 

  • Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V (2009) The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci USA 106(17):7173–7178

    CAS  Google Scholar 

  • Takatsuka Y, Nikaido H (2007) Site-directed disulfide cross-linking shows that cleft flexibility in the periplasmic domain is needed for the multidrug efflux pump AcrB of Escherichia coli. J Bacteriol 189(23):8677–8684

    CAS  Google Scholar 

  • Takatsuka Y, Nikaido H (2009) Covalently linked trimer of the AcrB multidrug efflux pump provides support for the functional rotating mechanism. J Bacteriol 191(6):1729–1737

    CAS  Google Scholar 

  • Tamura N, Murakami S, Oyama Y, Ishiguro M, Yamaguchi A (2005) Direct interaction of multidrug efflux transporter AcrB and outer membrane channel TolC detected via site-directed disulfide cross-linking. Biochemistry 44(33):11115–11121

    CAS  Google Scholar 

  • Thever MD, Saier MH Jr (2009) Bioinformatic characterization of P-type ATPases encoded within the fully sequenced genomes of 26 eukaryotes. J Membr Biol 229(3):115–130

    CAS  Google Scholar 

  • Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van der Lelie D (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182(5):1399–1409

    CAS  Google Scholar 

  • Tikhonova EB, Zgurskaya HI (2004) AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J Biol Chem 279(31):32116–32124

    CAS  Google Scholar 

  • Tikhonova EB, Devroy VK, Lau SY, Zgurskaya HI (2007) Reconstitution of the Escherichia coli macrolide transporter: the periplasmic membrane fusion protein MacA stimulates the ATPase activity of MacB. Mol Microbiol 63(3):895–910

    CAS  Google Scholar 

  • Tikhonova EB, Yamada Y, Zgurskaya HI (2011) Sequential mechanism of assembly of multidrug efflux pump AcrAB-TolC. Chem Biol 18(4):454–463

    CAS  Google Scholar 

  • Touze T, Eswaran J, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol Microbiol 53(2):697–706

    CAS  Google Scholar 

  • Trepout S, Taveau JC, Benabdelhak H, Granier T, Ducruix A, Frangakis AS, Lambert O (2010) Structure of reconstituted bacterial membrane efflux pump by cryo-electron tomography. Biochim Biophys Acta 1798(10):1953–1960

    CAS  Google Scholar 

  • Trepreau J, Girard E, Maillard AP, de Rosny E, Petit-Haertlein I, Kahn R, Covès J (2011) Structural basis for metal sensing by CnrX. J Mol Biol 408(4):766–779

    Google Scholar 

  • Trepreau J, Grosse C, Mouesca JM, Sarret G, Girard E, Petit-Haertlein I, Kuennemann S, Desbourdes C, de Rosny E, Maillard AP, Nies DH, Covès J (2014) Metal sensing and signal transduction by CnrX from Cupriavidus metallidurans CH34: role of the only methionine assessed by a functional, spectroscopic, and theoretical study. Metallomics 6(2):263–273

    Google Scholar 

  • Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MH Jr (1999) The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1(1):107–125

    CAS  Google Scholar 

  • Tsukazaki T, Mori H, Echizen Y, Ishitani R, Fukai S, Tanaka T, Perederina A, Vassylyev DG, Kohno T, Maturana AD, Ito K, Nureki O (2011) Structure and function of a membrane component SecDF that enhances protein export. Nature 474(7350):235–238

    CAS  Google Scholar 

  • Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17(9):849–850

    CAS  Google Scholar 

  • Vaccaro L, Koronakis V, Sansom MS (2006) Flexibility in a drug transport accessory protein: molecular dynamics simulations of MexA. Biophys J 91(2):558–564

    CAS  Google Scholar 

  • van der Lelie D, Schwuchow T, Schwidetzky U, Wuertz S, Baeyens W, Mergeay M, Nies DH (1997) Two-component regulatory system involved in transcriptional control of heavy-metal homoeostasis in Alcaligenes eutrophus. Mol Microbiol 23(3):493–503

    Google Scholar 

  • van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens aN, Schat H, Verkleij JA, Hooykaas PJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119 (3):1047–1055

    Google Scholar 

  • Van Houdt R, Monchy S, Leys N, Mergeay M (2009) New mobile genetic elements in Cupriavidus metallidurans CH34, their possible roles and occurrence in other bacteria. Anton Leeuw Int J G 96:205–226

    Google Scholar 

  • Van Houdt R, Monsieurs P, Mijnendonckx K, Provoost A, Janssen A, Mergeay M, Leys N (2012) Variation in genomic islands contribute to genome plasticity in Cupriavidus metallidurans. BMC Genom 13:111

    Google Scholar 

  • Van Houdt R, Toussaint A, Ryan MP, Pembroke JT, Mergeay M, Adley CC (2013) The Tn4371 ICE family of bacterial mobile genetic elements. In: Roberts AP, Mullany P (eds) Bacterial integrative mobile genetic elements. Landes Bioscience, Austin, pp 179–200

    Google Scholar 

  • Vargiu AV, Nikaido H (2012) Multidrug binding properties of the AcrB efflux pump characterized by molecular dynamics simulations. Proc Natl Acad Sci USA 109(50):20637–20642

    CAS  Google Scholar 

  • von Rozycki T, Nies DH (2009) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Anton Leeuw Int J G 96(2):115–139

    Google Scholar 

  • Wang K, Sitsel O, Meloni G, Autzen HE, Andersson M, Klymchuk T, Nielsen AM, Rees DC, Nissen P, Gourdon P (2014) Structure and mechanism of Zn2+-transporting P-type ATPases. Nature 514(7523):518–522

    CAS  Google Scholar 

  • Wei Y, Fu D (2005) Selective metal binding to a membrane-embedded aspartate in the Escherichia coli metal transporter YiiP (FieF). J Biol Chem 280(40):33716–33724

    CAS  Google Scholar 

  • Wei Y, Fu D (2006) Binding and transport of metal ions at the dimer interface of the Escherichia coli metal transporter YiiP. J Biol Chem 281(33):23492–23502

    CAS  Google Scholar 

  • Wei Y, Li H, Fu D (2004) Oligomeric state of the Escherichia coli metal transporter YiiP. J Biol Chem 279(38):39251–39259

    CAS  Google Scholar 

  • Welch A, Awah CU, Jing S, van Veen HW, Venter H (2010) Promiscuous partnering and independent activity of MexB, the multidrug transporter protein from Pseudomonas aeruginosa. Biochem J 430(2):355–364

    CAS  Google Scholar 

  • Wernimont AK, Huffman DL, Lamb AL, O’Halloran TV, Rosenzweig AC (2000) Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat Struct Biol 7(9):766–771

    CAS  Google Scholar 

  • Wiesemann N, Mohr J, Grosse C, Herzberg M, Hause G, Reith F, Nies DH (2013) Influence of copper resistance determinants on gold transformation by Cupriavidus metallidurans Strain CH34. J Bacteriol 195(10):2298–2308

    CAS  Google Scholar 

  • Wimmer R, Herrmann T, Solioz M, Wuthrich K (1999) NMR structure and metal interactions of the CopZ copper chaperone. J Biol Chem 274(32):22597–22603

    CAS  Google Scholar 

  • Wisedchaisri G, Park MS, Iadanza MG, Zheng H, Gonen T (2014) Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE. Nat Commun 5:4521

    CAS  Google Scholar 

  • Wu CC, Rice WJ, Stokes DL (2008) Structure of a copper pump suggests a regulatory role for its metal-binding domain. Structure 16(6):976–985

    CAS  Google Scholar 

  • Xu Y, Lee M, Moeller A, Song S, Yoon BY, Kim HM, Jun SY, Lee K, Ha NC (2011) Funnel-like hexameric assembly of the periplasmic adapter protein in the tripartite multidrug efflux pump in gram-negative bacteria. J Biol Chem 286(20):17910–17920

    CAS  Google Scholar 

  • Xue Y, Davis AV, Balakrishnan G, Stasser JP, Staehlin BM, Focia P, Spiro TG, Penner-Hahn JE, O’Halloran TV (2008) Cu(I) recognition via cation-pi and methionine interactions in CusF. Nat Chem Biol 4(2):107–109

    CAS  Google Scholar 

  • Yamaguchi A, Someya Y, Sawai T (1992) Metal-tetracycline/H+ antiporter of Escherichia coli encoded by transposon Tn10. The role of a conserved sequence motif, GXXXXRXGRR, in a putative cytoplasmic loop between helices 2 and 3. J Biol Chem 267(27):19155–19162

    CAS  Google Scholar 

  • Yamaguchi A, Kimura T, Someya Y, Sawai T (1993) Metal-tetracycline/H + antiporter of Escherichia coli encoded by transposon Tn10. The structural resemblance and functional difference in the role of the duplicated sequence motif between hydrophobic segments 2 and 3 and segments 8 and 9. J Biol Chem 268(9):6496–6504

    CAS  Google Scholar 

  • Yan N (2013) Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem Sci 38(3):151–159

    CAS  Google Scholar 

  • Yao XQ, Kimura N, Murakami S, Takada S (2013) Drug uptake pathways of multidrug transporter AcrB studied by molecular simulations and site-directed mutagenesis experiments. J Am Chem Soc 135(20):7474–7485

    CAS  Google Scholar 

  • Yoneyama H, Maseda H, Kamiguchi H, Nakae T (2000) Function of the membrane fusion protein, MexA, of the MexA, B-OprM efflux pump in Pseudomonas aeruginosa without an anchoring membrane. J Biol Chem 275(7):4628–4634

    CAS  Google Scholar 

  • Yu X, Carroll S, Rigaud JL, Inesi G (1993) H+ countertransport and electrogenicity of the sarcoplasmic reticulum Ca2+ pump in reconstituted proteoliposomes. Biophys J 64(4):1232–1242

    CAS  Google Scholar 

  • Yu L, Lu W, Wei Y (2011) AcrB trimer stability and efflux activity, insight from mutagenesis studies. PLoS ONE 6(12):e28390

    CAS  Google Scholar 

  • Yum S, Xu Y, Piao S, Sim SH, Kim HM, Jo WS, Kim KJ, Kweon HS, Jeong MH, Jeon H, Lee K, Ha NC (2009) Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. J Mol Biol 387(5):1286–1297

    CAS  Google Scholar 

  • Zgurskaya HI, Nikaido H (1999a) AcrA is a highly asymmetric protein capable of spanning the periplasm. J Mol Biol 285(1):409–420

    CAS  Google Scholar 

  • Zgurskaya HI, Nikaido H (1999b) Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc Natl Acad Sci USA 96(13):7190–7195

    CAS  Google Scholar 

  • Zgurskaya HI, Yamada Y, Tikhonova EB, Ge Q, Krishnamoorthy G (2009) Structural and functional diversity of bacterial membrane fusion proteins. Biochim Biophys Acta 1794(5):794–807

    CAS  Google Scholar 

  • Zoropogui A, Gambarelli S, Covès J (2008) CzcE from Cupriavidus metallidurans CH34 is a copper-binding protein. Biochem Biophys Res Commun 365(4):735–739

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for the Structure and Function of Biological Membranes, Center for Structural Biology and Bioinformatics, Université Libre de Bruxelles, Brussels, Belgium

    Guy Vandenbussche

  2. Unit Microbiology, Belgian Nuclear Research Centre (SCK•CEN), Mol, Belgium

    Max Mergeay & Rob Van Houdt

Authors
  1. Guy Vandenbussche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Max Mergeay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rob Van Houdt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guy Vandenbussche .

Rights and permissions

Reprints and permissions

Copyright information

© 2015 The Author(s)

About this chapter

Cite this chapter

Vandenbussche, G., Mergeay, M., Van Houdt, R. (2015). Metal Response in Cupriavidus metallidurans: Insights into the Structure-Function Relationship of Proteins. In: Metal Response in Cupriavidus metallidurans. SpringerBriefs in Molecular Science(). Springer, Cham. https://doi.org/10.1007/978-3-319-20624-0_1

Download citation

Publish with us

Policies and ethics

Search

Navigation