Abstract
This book chapter tries to visualize how a bacterial cell manages to bring zinc and no other transition metal cation to a zinc-dependent protein. Based upon the chemical constraints described in an introductory part of this book (“Chemical constraints for transition metal cation allocation” by author Dietrich H. Nies), a zinc allocation hypothesis was derived and tested on a theoretical level. The number of Lewis acids and bases were determined in the bacterium Cupriavidus metallidurans to define the stage. Molecular crowding and the Debye–Hückel equation describes how close the interacting Lewis bases and acids approach each other under cellular conditions. As one path for metal allocation, pre-discriminated cations may move along in the crowded areas from binding site to binding site, until “node” sites are reached that allow metal storage and discrimination by the formation of complex compounds. An inventory of motifs for such sites in C. metallidurans was derived. These may contribute to the movement of pre-discriminated ions or may be binding sites for already discriminated metals. As can be expected such motifs were found in proteins that are part of the three pillars of multiple metal homeostasis. First is the transportome, which adjusts the concentrations of metal cations and the composition of the mélange. Second is the repository, especially the zinc repository in the ribosome and RNA polymerase, which interacts with the transportome and buffers the cellular metal content. Third is a preference setting with iron first and sigma factors of the ECF (extracytoplasmic functions) family of sigma factors. This process is not completely understood at present.
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References
Ades SE, Grigorova IL, Gross CA (2003) Regulation of the alternative sigma factor sigma(E) during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli. J Bacteriol 185(8):2512–2519. https://doi.org/10.1128/Jb.185.8.2512-2519.2003
Affandi T, Issaian AV, McEvoy MM (2016) The structure of the periplasmic sensor domain of the histidine kinase CusS shows unusual metal ion coordination at the dimeric interface. Biochemist 55(37):5296–5306. https://doi.org/10.1021/acs.biochem.6b00707
Akanuma G, Nanamiya H, Natori Y, Nomura N, Kawamura F (2006) Liberation of zinc-containing L31 (RpmE) from ribosomes by its paralogous gene product, YtiA, in Bacillus subtilis. J Bacteriol 188:2715–2720
Altendorf K, Epstein W (1996) The Kdp-ATPase of Escherichia coli. In: Dalbey RE (ed) Advances in cell and molecular biology of membranes and organelles, vol 5. JAI Press, Greenwich, pp 401–418
Ammendola S, Ciavardelli D, Consalvo A, Battistoni A (2020) Cobalt can fully recover the phenotypes related to zinc deficiency in Salmonella typhimurium. Metallomics 12(12):2021–2031. https://doi.org/10.1039/d0mt00145g
Argüello JM, Eren E, Gonzalez-Guerrero M (2007) The structure and function of heavy metal transport P-1B-ATPases. Biometals 20:233–248
Atanassova A, Zamble DB (2005) Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J Bacteriol 187(14):4689–4697
Baichoo N, Helmann JD (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184:5826–5832
Banaszak K, Martin-Diaconescu V, Bellucci M, Zambelli B, Rypniewski W, Maroney MJ, Ciurli S (2012) Crystallographic and X-ray absorption spectroscopic characterization of Helicobacter pylori UreE bound to Ni2+ and Zn2+ reveals a role for the disordered C-terminal arm in metal trafficking. Biochem J 441:1017–1026. https://doi.org/10.1042/bj20111659
Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P (2010) Affinity gradients drive copper to cellular destinations. Nature 465(7298):645–648. https://doi.org/10.1038/nature09018
Bartha R, Ordal EJ (1965) Nickel-dependent chemolithotrophic growth of two Hydrogenomonas strains. J Bacteriol 89:1015–1019
Beard SJ, Hashim R, Wu GH, Binet MRB, Hughes MN, Poole RK (2000) Evidence for the transport of zinc(II) ions via the Pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiol Lett 184(2):231–235
Bellucci M, Zambelli B, Musiani F, Turano P, Ciurli S (2009) Helicobacter pylori UreE, a urease accessory protein: specific Ni2+- and Zn2+-binding properties and interaction with its cognate UreG. Biochem J 422:91–100. https://doi.org/10.1042/bj20090434
Benanti EL, Chivers PT (2009) An intact urease assembly pathway is required to compete with NikR for nickel ions in Helicobacter pylori. J Bacteriol 191(7):2405–2408. https://doi.org/10.1128/jb.01657-08
Bender CL, Cooksey DA (1985) Plasmid-mediated copper resistance in Pseudomonas syringae pv tomato. Phytopathology 75(11):1325–1325
Bersch B, Favier A, Schanda P, van Aelst S, Vallaeys T, Coves 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
Bjerrum N (1926) Untersuchungen über Ionenassoziation. In: I. Der Einfluss der Ionenassoziation auf die Aktivität der Ionen bei Mittleren Assoziationsgraden. Publisher B. Lunos, Copenhagen
Bleichert P, Bütof L, Rückert C, Herzberg M, Francisco R, Morais P, Grass G, Kalinowski J, Nies DH (2021) Mutant strains of Escherichia coli and methicillin-resistant Staphylococcus aureus obtained by laboratory selection to survive on metallic copper surfaces. Appl Environ Microbiol 87(1):e01788–e01720. https://doi.org/10.1128/AEM.01788-20
Bobrov AG, Kirillina O, Fetherston JD, Miller MC, Burlison JA, Perry RD (2014) The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice. Mol Microbiol 93(4):759–775. https://doi.org/10.1111/mmi.12693
Borremans B, Hobman JL, Provoost A, Brown NL, Van der Lelie D (2001) Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J Bacteriol 183(19):5651–5658
Braun V (1995) Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol Rev 16(4):295–307
Braun V, Braun M (2002) Active transport of iron and siderophore antibiotics. Curr Opin Microbiol 5:194–201
Brazelton WJ, Morrill PL, Szponar N, Schrenk MO (2013) Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl Environ Microbiol 79(13):3906–3916. https://doi.org/10.1128/AEM.00330-13
Brown NL, Barrett SR, Camakaris J, Lee BT, Rouch DA (1995) Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. Mol Microbiol 17(6):1153–1166
Burgess J (1978) Chapter 12: Kinetics and mechanism: complex formation. In: Metal ions in solution. Ellis Horwood, Chichester
Burmann BM, Schweimer K, Luo X, Wahl MC, Stitt BL, Gottesman ME, Rosch P (2010) A NusE:NusG complex links transcription and translation. Science 328(5977):501–504. https://doi.org/10.1126/science.1184953
Bütof L, Schmidt-Vogler C, Herzberg M, Große C, Nies DH (2017) The components of the unique Zur regulon of Cupriavidus metallidurans mediate cytoplasmic zinc handling. J Bacteriol 199(21):e00372–e00317., spotlight article. https://doi.org/10.1128/JB.00372-17
Bütof L, Wiesemann N, Herzberg M, Altzschner M, Holleitner A, Reith F, Nies DH (2018) Synergetic gold-copper detoxification at the core of gold biomineralisation in Cupriavidus metallidurans. Metallomics 10:278–286. https://doi.org/10.1039/c7mt00312a
Bütof L, Große C, Lilie H, Herzberg M, Nies DH (2019) Interplay between the Zur regulon components and metal resistance in Cupriavidus metallidurans. J Bacteriol 201(15):e00192–e00119. https://doi.org/10.1128/JB.00192-19
Cerasi M, Liu JZ, Ammendola S, Poe AJ, Petrarca P, Pesciaroli M, Pasquali P, Raffatellu M, Battistoni A (2014) The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence. Metallomics 6(4):845–853. https://doi.org/10.1039/c3mt00352c
Cha JS, Cooksey DA (1991) Copper resistance in pseudomonas-syringae mediated by periplasmic and outer-membrane proteins. Proc Natl Acad Sci U S A 88(20):8915–8919. https://doi.org/10.1073/pnas.88.20.8915
Chandrangsu P, Huang X, Gaballa A, Helmann JD (2019) Bacillus subtilis FolE is sustained by the ZagA zinc metallochaperone and the alarmone ZTP under conditions of zinc deficiency. Mol Microbiol 112:751–765
Changela A, Chen K, Xue Y, Holschen J, Outten CE, O’Halloran TV, Mondragon A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301(5638):1383–1387
Chao Y, Fu D (2004) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279(17):17173–17180
Cheng TF, Li HY, Yang XM, **a W, Sun HZ (2013) Interaction of SlyD with HypB of Helicobacter pylori facilitates nickel trafficking. Metallomics 5(7):804–807. https://doi.org/10.1039/c3mt00014a
Choi E, Groisman EA, Shin D (2009) Activated by different signals, the PhoP/PhoQ two-component system differentially regulates metal uptake. J Bacteriol 191(23):7174–7181. https://doi.org/10.1128/JB.00958-09
Colvin RA, Holmes WR, Fontaine CP, Maret W (2010) Cytosolic zinc buffering and muffling: Their role in intracellular zinc homeostasis. Metallomics 2(5):306–317. https://doi.org/10.1039/b926662c
Cooksey DA (1993) Copper uptake and resistance in bacteria. Mol Microbiol 7(1):1–5. https://doi.org/10.1111/j.1365-2958.1993.tb01091.x
Coulton JW, Mason P, Cameron DR, Carmel G, Jean R, Rode HN (1986) Protein fusions of beta-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol 165(1):181–192
Dawson RMC, Elliott DC, Elliott WH, Jones KM (1969) Data for biochemical research, 2nd edn. At The Clarendon Press, Oxford
De Angelis F, Lee JK, O’Connell JD, Miercke LJW, 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 U S A 107(24):11038–11043. https://doi.org/10.1073/Pnas.1003908107
Debye P, Hückel E (1923) Zur Theorie der Elektrolyte. I. Gefrierpunktserniedrigung und verwandte Erscheinungen. Phys Z 24:185–206
Diels L, Mergeay M (1990) DNA probe-mediated detection of resistant bacteria from soils highy polluted by heavy metals. Appl Environ Microbiol 56:1485–1491
Douglas CD, Ngu TT, Kaluarachchi H, Zamble DB (2013) Metal transfer within the Escherichia coli HypB-HypA complex of hydrogenase accessory proteins. Biochemist 52(35):6030–6039. https://doi.org/10.1021/bi400812r
Eberz G, Eitinger T, Friedrich B (1989) Genetic determinants of a nickel-specific transport system are part of the plasmid-encoded hydrogenase gene cluster in Alcaligenes eutrophus. J Bacteriol 171:1340–1345
Egler M, Große C, Grass G, Nies DH (2005) Role of ECF sigma factor RpoE in heavy metal resistance of Escherichia coli. J Bacteriol 187:2297–2307
Eitinger T, Friedrich B (1991) Cloning, nucleotide sequence, and heterologous expression of a high-affinity nickel transport gene from Alcaligenes eutrophus. J Biol Chem 266(5):3222–3227
Eitinger T, Friedrich B (1994) A topological model for the high-affinity nickel transporter of Alcaligenes eutrophus. Mol Microbiol 12(6):1025–1032
Eitinger T, Wolfram L, Degen O, Anthon C (1997) A Ni2+ binding motif is the basis of high affinity transport of the Alcaligenes eutrophus nickel permease. J Biol Chem 272(27):17139–17144
Eitinger T, Suhr J, Moore L, Smith JAC (2005) Secondary transporters for nickel and cobalt ions: Theme and variations. Biometals 18(4):399–405
Eitinger T, Rodionov DA, Grote M, Schneider E (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev 35(1):3–67. https://doi.org/10.1111/j.1574-6976.2010.00230.x
Eshaghi S, Niegowski D, Kohl A, Molina DM, Lesley SA, Nordlund P (2006) Crystal structure of a divalent metal ion transporter CorA at 2.9 angstrom resolution. Science 313(5785):354–357
Fagan MJ, Saier MH Jr (1994) P-type ATPases of eukaryotes and bacteria: sequence comparisons and construction of phylogenetic trees. J Mol Evol 38:57–99
Fantino JR, Py B, Fontecave M, Barras F (2010) A genetic analysis of the response of Escherichia coli to cobalt stress. Environ Microbiol 12(10):2846–2857. https://doi.org/10.1111/j.1462-2920.2010.02265.x
Farrugia MA, Macomber L, Hausinger RP (2013) Biosynthesis of the urease metallocenter. J Biol Chem 288(19):13178–13185. https://doi.org/10.1074/jbc.R112.446526
Farrugia MA, Wang BB, Feig M, Hausinger RP (2015) Mutational and computational evidence that a nickel-transfer tunnel in UreD is used for activation of Klebsiella aerogenes urease. Biochemist 54(41):6392–6401. https://doi.org/10.1021/acs.biochem.5b00942
Fath MJ, Kolter R (1993) ABC-transporters: the bacterial exporters. Microbiol Rev 57:995–1017
Feklistov A, Sharon BD, Darst SA, Gross CA (2014) Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 68:357–376. https://doi.org/10.1146/annurev-micro-092412-155737
Fischer N, Neumann P, Konevega AL, Bock LV, Ficner R, Rodnina MV, Stark H (2015) Structure of the E. coli ribosome-EF-Tu complex at <3 A resolution by Cs-corrected cryo-EM. Nature 520(7548):567–570. https://doi.org/10.1038/nature14275
Fong YH, Wong HC, Chuck CP, Chen YW, Sun HZ, Wong KB (2011) Assembly of preactivation complex for urease maturation in Helicobacter pylori. Crystal structure of the UreF-UreH protein complex. J Biol Chem 286(50):43241–43249. https://doi.org/10.1074/jbc.M111.296830
Fong YH, Wong HC, Yuen MH, Lau PH, Chen YW, Wong KB (2013) Structure of UreG/UreF/UreH complex reveals how urease accessory proteins facilitate maturation of Helicobacter pylori urease. PLoS Biol 11(10):e100167810
Fontenot CR, Tasnim H, Valdes KA, Popescu CV, Ding H (2020) Ferric uptake regulator (Fur) reversibly binds a [2Fe-2S] cluster to sense intracellular iron homeostasis in Escherichia coli. J Biol Chem 295(46):15454–15463. https://doi.org/10.1074/jbc.RA120.014814
Fu CL, Olson JW, Maier RJ (1995) HypB protein of Bradyrhizobium japonicum Is a metal-binding GTPase capable of binding 18 divalent nickel ions per dimer. Proc Natl Acad Sci U S A 92(6):2333–2337. https://doi.org/10.1073/pnas.92.6.2333
Gaballa A, Helmann JD (1998) Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180(22):5815–5821
Gabriel SE, Helmann JD (2009) Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J Bacteriol 191(19):6116–6122. https://doi.org/10.1128/jb.00802-09
Garrick MD, Singleton ST, Vargas F, Kuo HC, Zhao L, Knopfel M, Davidson T, Costa M, Paradkar P, Roth JA, Garrick LM (2006) DMTI: Which metals does it transport? Biol Res 39(1):79–85
Gasper R, Scrima A, Wittinghofer A (2006) Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 281(37):27492–27502
Goldberg M, Pribyl T, Juhnke S, Nies DH (1999) Energetics and topology of CzcA, a cation/proton antiporter of the RND protein family. J Biol Chem 274:26065–26070
Gonzalez-Guerrero M, Raimunda D, Cheng X, Argüello JM (2010) Distinct functional roles of homologous Cu plus efflux ATPases in Pseudomonas aeruginosa. Mol Microbiol 78(5):1246–1258. https://doi.org/10.1111/j.1365-2958.2010.07402.x
Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, Mergeay M, Kersters K, Vandamme P (2001) Classification of metal-resistant bacteria from industrial biotopes as Ralstonia campinensis sp. nov., Ralstonia metallidurans sp. nov. and Ralstonia basilensis Steinle et al. 1998 emend. Int J Syst Evol Microbiol 51:1773–1782
Grass G, Rensing C (2001) CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun 286(5):902–908
Grass G, Große C, Nies DH (2000) Regulation of the cnr cobalt/nickel resistance determinant from Ralstonia sp. CH34. J Bacteriol 182(5):1390–1398
Grass G, Wong MD, Rosen BP, Smith RL, Rensing C (2002) ZupT Is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184:864–866
Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005a) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611
Grass G, Fricke B, Nies DH (2005b) Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals 18:437–448
Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005c) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183(1):9–18
Gregg CM, Goetzl S, Jeoung JH, Dobbek H (2016) AcsF catalyzes the ATP-dependent insertion of nickel into the Ni,Ni-[4Fe4S] cluster of acetyl-CoA synthase. J Biol Chem 291(35):18129–18138. https://doi.org/10.1074/jbc.M116.731638
Große C, Grass G, Anton A, Franke S, Navarrete Santos A, Lawley B, Brown NL, Nies DH (1999) Transcriptional organization of the czc heavy metal homoeostasis determinant from Alcaligenes eutrophus. J Bacteriol 181:2385–2393
Große C, Friedrich S, Nies DH (2007) Contribution of extracytoplasmic function sigma factors to transition metal homeostasis in Cupriavidus metallidurans strain CH34. J Mol Microbiol Biotechnol 12:227–240
Große C, Schleuder G, Schmole C, Nies DH (2014) Survival of Escherichia coli cells on solid copper surfaces is increased by glutathione. Appl Environ Microbiol 80(22):7071–7078. https://doi.org/10.1128/AEM.02842-14
Grosse C, Herzberg M, Schüttau M, Nies DH (2016) Characterization of the Δ7 mutant of Cupriavidus metallidurans with deletions of seven secondary metal uptake systems. mSystems 1(1):e00004–e00016. https://doi.org/10.1128/mSystems.00004-16
Große C, Poehlein A, Blank K, Schwarzenberger C, Schleuder G, Herzberg M, Nies DH (2019) The third pillar of metal homeostasis in Cupriavidus metallidurans CH34: Preferences are controlled by extracytoplasmic functions sigma factors. Metallomics 11:291–316. https://doi.org/10.1039/C8MT00299A
Große C, Kohl T, Herzberg M, Nies DH (2022) Loss of mobile genomic islands in metal resistant, hydrogen-oxidizing Cupriavidus metallidurans. Appl Environ Microbiol 88:e02048-21. https://doi.org/10.1128/aem.02048-21
Guan G, Pinochet-Barros A, Gaballa A, Patel SJ, Arguello JM, Helmann JD (2015) PfeT, a P1B4 -type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication. Mol Microbiol 98(4):787–803. https://doi.org/10.1111/mmi.13158
Gudipaty SA, McEvoy MM (2014) The histidine kinase CusS senses silver ions through direct binding by its sensor domain. Biochimica Et Biophysica Acta-Proteins and Proteomics 1844(9):1656–1661. https://doi.org/10.1016/j.bbapap.2014.06.001
Gudipaty SA, Larsen AS, Rensing C, McEvoy MM (2012) Regulation of Cu(I)/Ag(I) efflux genes in Escherichia coli by the sensor kinase CusS. FEMS Microbiol Lett 330(1):30–37. https://doi.org/10.1111/j.1574-6968.2012.02529.x
Guskov A, Nordin N, Reynaud A, Engman H, Lundback AK, Jong AJO, Cornvik T, Phua T, Eshaghi S (2012) Structural insights into the mechanisms of Mg2+ uptake, transport, and gating by CorA. Proc Natl Acad Sci U S A 109(45):18459–18464. https://doi.org/10.1073/pnas.1210076109
Haas CE, Rodionov DA, Kropat J, Malasarn D, Merchant SS, de Crecy-Lagard V (2009) A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10:470. https://doi.org/10.1186/1471-2164-10-470
Hantke K (1983) Identification of an iron uptake system specific for coprogen and rhodotorulic acid in Escherichia coli K12. Mol Gen Genet 191(2):301–306
Hantke K (1987) Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol Gen Genet 210:135–139. https://doi.org/10.1007/BF00337769
Hantke K (2005) Bacterial zinc uptake and regulators. Curr Opin Microbiol 8(2):196–202
Harden TT, Wells CD, Friedman LJ, Landick R, Hochschild A, Kondev J, Gelles J (2016) Bacterial RNA polymerase can retain sigma70 throughout transcription. Proc Natl Acad Sci U S A 113(3):602–607. https://doi.org/10.1073/pnas.1513899113
Harris RM, Webb DC, Howitt SM, Cox GB (2001) Characterization of PitA and PitB from Escherichia coli. J Bacteriol 183(17):5008–5014. https://doi.org/10.1128/Jb.183.17.5008-5014.2001
Hashemian S (2011) Interaction energies of histidine with cations (H+, Li+, Na+, K+, Mg2+, Ca2+). Russ J Inorg Chem 56(3):397–401. https://doi.org/10.1134/s0036023611020082
Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110
Helmann JD, Soonsange S, Gabriel S (2007) Metallalloregulators: arbiters of metal sufficiency. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals, Microbiology Monographs, vol 6. Springer-Verlag, Berlin, pp 37–71
Hensley MP, Tierney DL, Crowder MW (2011) Zn(II) binding to Escherichia coli 70S ribosomes. Biochemist 50(46):9937–9939. https://doi.org/10.1021/bi200619w
Herzberg M, Bauer L, Nies DH (2014a) Deletion of the zupT gene for a zinc importer influences zinc pools in Cupriavidus metallidurans CH34. Metallomics 6:421–436. https://doi.org/10.1039/C3MT00267E
Herzberg M, Dobritzsch D, Helm S, Baginski S, Nies DH (2014b) The zinc repository of Cupriavidus metallidurans. Metallomics 6:2157–2165. https://doi.org/10.1039/C4MT00171K
Herzberg M, Schüttau M, Reimers M, Grosse C, Schlegel HG, Nies DH (2015) Synthesis of nickel-iron hydrogenase in Cupriavidus metallidurans is controlled by metal-dependent silencing and un-silencing of genomic islands. Metallomics 7:632–649. https://doi.org/10.1039/C4MT00297K
Herzberg M, Bauer L, Kirsten A, Nies DH (2016) Interplay between seven secondary metal transport systems is required for full metal resistance of Cupriavidus metallidurans. Metallomics 8:313–326. https://doi.org/10.1039/C5MT00295H
Higgins CF (1992) ABC-transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
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 U S A 101(27):9994–9999
Higgs PI, Myers PS, Postle K (1998) Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J Bacteriol 180(22):6031–6038
Hobman JL, Yamamoto K, Oshima T (2007) Transcriptomic responses of bacterial cells to sublethal metal ion stress. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals, vol 6. Springer-Verlag, Berlin, pp 73–116
Housecroft CE, Constable EC (2006) Chemistry, 3rd edn. Pearson Education, Essex
Hubbard PA, Padovani D, Labunska T, Mahlstedt SA, Banerjee R, Drennan CL (2007) Crystal structure and mutagenesis of the metallochaperone MeaB - Insight into the causes of methylmalonic aciduria. J Biol Chem 282(43):31308–31316
Hunte C, Screpanti E, Venturi M, Rimon A, Padan E, Michel H (2005) Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435:1197–1202
Ishihama A (1988) Promoter selectivity of prokaryotic RNA polymerases. Trends Genet 4:282–286
Israelachvili J (1985) Intermolecular and surface forces. Academic Press, Cambridge MA
Jackson RJ, Binet MRB, Lee LJ, Ma R, Graham AI, McLeod CW, Poole RK (2008) Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels. FEMS Microbiol Lett 289(2):219–224. https://doi.org/10.1111/j.1574-6968.2008.01386.x
Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Medigue 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. https://doi.org/10.1371/journal.pone.0010433
Jeon WB, Cheng JJ, Ludden PW (2001) Purification and characterization of membrane-associated CooC protein and its functional role in the insertion of nickel into carbon monoxide dehydrogenase from Rhodospirillum rubrum. J Biol Chem 276(42):38602–38609
Jeoung JH, Giese T, Grunwald M, Dobbek H (2009) CooC1 from Carboxydothermus hydrogenoformans is a nickel-binding ATPase. Biochemist 48(48):11505–11513. https://doi.org/10.1021/bi901443z
Jian X, Wasinger EC, Lockard JV, Chen LX, He C (2009) Highly sensitive and selective gold(I) recognition by a metalloregulator in Ralstonia metallidurans. J Amer Chem Soc 131:10869–10871
Johnson RC, Hu HQ, Merrell DS, Maroney MJ (2015) Dynamic HypA zinc site is essential for acid viability and proper urease maturation in Helicobacter pylori. Metallomics 7(4):674–682. https://doi.org/10.1039/c4mt00306c
Juhnke S, Peitzsch N, Hübener N, Große C, Nies DH (2002) New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch Microbiol 179:15–25
Junge W, Sielaff H, Engelbrecht S (2009) Torque generation and elastic power transmission in the rotary F(O)F(1)-ATPase. Nature 459(7245):364–370. https://doi.org/10.1038/nature08145
Kamizomo A, Nishizawa M, Teranishi A, Murata K, Kimura A (1989) Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol Gen Genet 219:161–167
Kanehisa M, Sato Y (2020) KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci 29(1):28–35. https://doi.org/10.1002/pro.3711
Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–D357
Karp P, Weaver D, Paley S, Fulcher C, Kubo A, Kothari A, Krummenacker M, Subhraveti P, Weerasinghe D, Gama-Castro S, Huerta A, Muñiz-Rascado L, Bonavides-Martinez C, Weiss V, Peralta-Gil M, Santos-Zavaleta A, Schröder I, Mackie A, Gunsalus R, Collado-Vides J, Keseler I, Paulsen I (2014) The EcoCyc Database. EcoSal Plus. https://doi.org/10.1128/ecosalplus.ESP-0009-2013
Kean J, Cleverley RM, O’Ryan L, Ford RC, Prince SM, Derrick JP (2008) Characterization of a CorA Mg2+transport channel from Methanococcus jannaschii using a thermofluor-based stability assay. Mol Membr Biol 25(8):653–661. https://doi.org/10.1080/09687680802541169
Kehres DG, Zaharik ML, Finlay BB, Maguire ME (2000) The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36(5):1085–1100
Kerby RL, Ludden PW, Roberts GP (1997) In vivo nickel insertion into the carbon monoxide dehydrogenase of Rhodospirillum rubrum: Molecular and physiological characterization of cooCTJ. J Bacteriol 179(7):2259–2266. https://doi.org/10.1128/jb.179.7.2259-2266.1997
Khil PP, Obmolova G, Teplyakov A, Howard AJ, Gilliland GL, Camerini-Otero RD (2004) Crystal structure of the Escherichia coli YjiA protein suggests a GTP-dependent regulatory function. Proteins 54(2):371–374. https://doi.org/10.1002/prot.10430
Khorasani-Motlagh M, Lacasse MJ, Zamble DB (2017) High-affinity metal binding by the Escherichia coli [NiFe]-hydrogenase accessory protein HypB is selectively modulated by SlyD. Metallomics 9(5):482–493. https://doi.org/10.1039/c7mt00037e
Kim E-H, Nies DH, McEvoy M, Rensing C (2011) Switch oder funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 193:2381–2387. https://doi.org/10.1128/JB.01323-10
Kirsten A, Herzberg M, Voigt A, Seravalli J, Grass G, Scherer J, Nies DH (2011) Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34. J Bacteriol 193(18):4652–4663
Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37(2):239–253. https://doi.org/10.1046/j.1365-2958.2000.01983.x
Kohler R, Mooney RA, Mills DJ, Landick R, Cramer P (2017) Architecture of a transcribing-translating expressome. Science 356(6334):194–197. https://doi.org/10.1126/science.aal3059
Krezel A, Maret W (2016) The biological inorganic chemistry of zinc ions. Arch Biochem Biophys 611:3–19. https://doi.org/10.1016/j.abb.2016.04.010
Kühlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295. https://doi.org/10.1038/nrm1354
Kumar BA, Naik KB, Raju S, Rao GN (2015) Formation and confirmation of binary complexes of calcium(II), magnesium(II) and zinc(II) with L-histidine in dioxan-water media. Chem Spec Bioavailability 24(3):139–146. https://doi.org/10.3184/095422912x13406452149755
Lacasse MJ, Zamble DB (2016) [NiFe]-Hydrogenase Maturation. Biochemist 55(12):1689–1701. https://doi.org/10.1021/acs.biochem.5b01328
Lacasse MJ, Douglas CD, Zamble DB (2016) Mechanism of selective nickel transfer from HypB to HypA, Escherichia coli [NiFe]-hydrogenase accessory proteins. Biochemist 55(49):6821–6831. https://doi.org/10.1021/acs.biochem.6b00706
Leach MR, Zhang JW, Zamble DB (2007) The role of complex formation between the Escherichia coli hydrogenase accessory factors HypB and SlyD. J Biol Chem 282(22):16177–16186
Legatzki A, Anton A, Grass G, Rensing C, Nies DH (2003a) Interplay of the Czc-system and two P-type ATPases in conferring metal resistance to Ralstonia metallidurans. J Bacteriol 185:4354–4361
Legatzki A, Franke S, Lucke S, Hoffmann T, Anton A, Neumann D, Nies DH (2003b) First step towards a quantitative model describing Czc-mediated heavy metal resistance in Ralstonia metallidurans. Biodegradation 14:153–168
Lehninger AL (1977) Biochemistry. Worth Publishers, New York
Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317(1):41–72. https://doi.org/10.1006/jmbi.2001.5378
Li Y, Sharma MR, Koripella RK, Banavali NK, Agrawal RK, Ojha AK (2021) Ribosome hibernation: a new molecular framework for targeting nonreplicating persisters of mycobacteria. Microbiology 167(2):001035. https://doi.org/10.1099/mic.0.001035
Liesegang H, Lemke K, Siddiqui RA, Schlegel H-G (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175:767–778
Lonetto MA, Brown KL, Rudd KE, Buttner MJ (1994) Analysis of the Streptomyces coelicolor sigF gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A 91:7573–7577
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. https://doi.org/10.1038/Nature09395
Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317(5845):1746–1748
Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nature Struc Mol Biol 16(10):1063–1068. https://doi.org/10.1038/nsmb.1662
Lucarelli D, Russo S, Garman E, Milano A, Meyer-Klaucke W, Pohl E (2007) Crystal structure and function of the zinc uptake regulator FurB from Mycobacterium tuberculosis. J Biol Chem 282(13):9914–9922
Lunin V, Dobrovetsky E, Khutoreskaya G, Zhang R, Joachimiak A, Doyle DA, Bochkarev A, Maguire ME, Edwards AM, Koth CM (2006) Crystal structure of the CorA Mg2+ transporter. Nature 440:833–837
Ma Z, Gabriel SE, Helmann JD (2011) Sequential binding and sensing of Zn(II) by Bacillus subtilis Zur. Nucleic Acids Res 39(21):9130–9138. https://doi.org/10.1093/nar/gkr625
Magnani D, Solioz M (2007) How bacteria handle copper. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals, Microbiology monographs, vol 6. Springer-Verlag, Berlin, pp 259–285
Maier T, Jacobi A, Sauter M, Böck A (1993) The product of the hypB gene, which Is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175(3):630–635
Maillard AP, Girard E, Ziani W, Petit-Hartlein I, Kahn R, Coves 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. https://doi.org/10.1016/j.jmb.2014.04.003
Maillard AP, Kuennemann S, Grosse C, Volbeda A, Schleuder G, Petit-Härtlein I, de Rosny E, Nies DH, Coves J (2015) Response of CnrX from Cupriavidus metallidurans CH34 to nickel binding. Metallomics 7:622–631. https://doi.org/10.1039/c4mt00293h
Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF (2000) Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35(5):1065–1078
Markov D, Naryshkina T, Mustaev A, Severinov K (1999) A zinc-binding site in the largest subunit of DNA-dependent RNA polymerase is involved in enzyme assembly. Genes Dev 13(18):2439–2448
Martin-Diaconescu V, Joseph CA, Boer JL, Mulrooney SB, Hausinger RP, Maroney MJ (2017) Non-thiolate ligation of nickel by nucleotide-free UreG of Klebsiella aerogenes. J Biol Inorg Chem 22(4):497–503. https://doi.org/10.1007/s00775-016-1429-9
Mazzon RR, Braz VS, da Silva Neto JF, do Valle Marques M (2014) Analysis of the Caulobacter crescentus Zur regulon reveals novel insights in zinc acquisition by TonB-dependent outer membrane proteins. BMC Genomics 15:1–14
McCarthy S, Ai C, Wheaton G, Tevatia R, Eckrich V, Kelly R, Blum P (2014) Role of an archaeal PitA transporter in the copper and arsenic resistance of Metallosphaera sedula, an extreme thermoacidophile. J Bacteriol 196(20):3562–3570. https://doi.org/10.1128/jb.01707-14
McMillan DJ, Mau M, Walker MJ (1998) Characterisation of the urease gene cluster in Bordetella bronchiseptica. Gene 208(2):243–251. https://doi.org/10.1016/S0378-1119(97)00651-3
Mehta N, Olson JW, Maier RJ (2003) Characterization of Helicobacter pylori nickel metabolism accessory proteins needed for maturation of both urease and hydrogenase. J Bacteriol 185(3):726–734
Mellano MA, Cooksey DA (1988) Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. tomato. J Bacteriol 170(6):2879–2883
Mergeay M (2000) Bacteria adapted to industrial biotopes: metal-resistant Ralstonia. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington DC, pp 403–414
Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334
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
Merloni A, Dobrovolska O, Zambelli B, Agostini F, Bazzani M, Musiani F, Ciurli S (2014) Molecular landscape of the interaction between the urease accessory proteins UreE and UreG. Biochimica Et Biophysica Acta-Proteins and Proteomics 1844(9):1662–1674. https://doi.org/10.1016/j.bbapap.2014.06.016
Missiakas D, Raina S (1998) The extracytoplasmic function sigma factors: role and regulation. Mol Microbiol 28:1059–1066
Mohapatra S, Weisshaar JC (2018) Functional map** of the E. coli translational machinery using single-molecule tracking. Mol Microbiol 110(2):262–282. https://doi.org/10.1111/mmi.14103
Monchy S, Benotmane MA, Wattiez R, van Aelst S, Auquier V, Borremans B, Mergeay M, Taghavi S, van der Lelie D, Vallaeys T (2006) Transcriptomics and proteomic analysis of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152:1765–1776
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 186:8036–8043
Nies DH (1992) CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc and cadmium (czc system) in Alcaligenes eutrophus. J Bacteriol 174:8102–8110
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 177:2707–2712
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2/3):313–339
Nies DH (2004) Incidence and function of sigma factors in Ralstonia metallidurans and other bacteria. Arch Microbiol 181:255–268
Nies DH (2007a) Bacterial transition metal homeostasis. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals, Microbiology monographs, vol 6. Springer-Verlag, Berlin, pp 118–142
Nies DH (2007b) How cells control zinc homeostasis. Science 317:1695–1696
Nies DH (2013) RND-efflux pumps for metal cations. In: Yu EW, Zhang Q, Brown MH (eds) Microbial efflux pumps: current research. Caister Academic Press, Norfolk, pp 79–122. ISBN: 978-1-908230-21-8
Nies DH (2014) Basic biochemical roots. In: Ecological biochemistry: environmental and interspecies interactions. Wiley-VCH, Weinheim
Nies DH (2016) The biological chemistry of the transition metal “transportome” of Cupriavidus metallidurans. Metallomics 8:481–507. https://doi.org/10.1039/C5MT00320B
Nies DH (2019) The ancient alarmone ZTP and zinc homeostasis in Bacillus subtilis. Mol Microbiol 112:741–746. https://doi.org/10.1111/mmi.14332
Nies DH, Brown N (1998) Two-component systems in the regulation of heavy metal resistance. In: Silver S, Walden W (eds) Metal ions in gene regulation. Chapman Hall, New York, pp 77–103
Nies DH, Silver S (1989) Plasmid-determined inducible efflux is responsible for resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus. J Bacteriol 171:896–900
Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199
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 169:4865–4868
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 U S A 86:7351–7355
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 Micobiol Biotechnol 11:82–93
Nies DH, Coves J, Sawers G (2017) Cross-talk between nickel and other metals in microbial systems. In: Kozłowski H, Zamble D, Rowińska-Żyrek M (eds) The Biochem of Nickel. The Royal Society of Chemistry, London, pp 306–338
Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60. https://doi.org/10.1146/annurev.micro.112408.134247
Nordin N, Guskov A, Phua T, Sahaf N, **a Y, Lu SY, Eshaghi H, Eshaghi S (2013) Exploring the structure and function of Thermotoga maritime CorA reveals the mechanism of gating and ion selectivity in Co2+/Mg2+ transport. Biochem J 451:365–374. https://doi.org/10.1042/bj20121745
Norris V, den Blaauwen T, Cabin-Flaman A, Doi RH, Harshey R, Janniere L, Jimenez-Sanchez A, ** DJ, Levin PA, Mileykovskaya E, Minsky A, Saier M Jr, Skarstad K (2007) Functional taxonomy of bacterial hyperstructures. Microbiol Mol Biol Rev 71(1):230–253. https://doi.org/10.1128/MMBR.00035-06
O’Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275(33):25057–25060
Olson JW, Mehta NS, Maier RJ (2001) Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol Microbiol 39(1):176–182
Outten FW, Huffman DL, Hale JA, O’Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276(33):30670–30677
Owen GA, Pascoe B, Kallifidas D, Paget MSB (2007) Zinc-responsive regulation of alternative ribosomal protein genes in Streptomyces coelicolor involves Zur and sigma(R). J Bacteriol 189(11):4078–4086
Padan E, Venturi M, Gerchman Y, Dover N (2001) Na+/H+ antiporters. Biochim Biophys Acta 1505:144–157
Panina EM, Mironov AA, Gelfand MS (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci U S A 100(17):9912–9917
Papp-Wallace KM, Nartea M, Kehres DG, Porwollik S, McClelland M, Libby SJ, Fang FC, Maguire ME (2008) The CorA Mg2+ channel is required for the virulence of Salmonella enterica serovar Typhimurium. J Bacteriol 190(19):6517–6523. https://doi.org/10.1128/JB.00772-08
Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28(6):1199–1210
Paulsen IT, Saier MH Jr (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156(2):99–103
Paulsen IT, Park JH, Choi PS, Saier MHJ (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 156:1–8
Pfoh R, Li A, Chakrabarti N, Payandeh J, Pomes R, Pai EF (2012) Structural asymmetry in the magnesium channel CorA points to sequential allosteric regulation. Proc Natl Acad Sci U S A 109(46):18809–18814. https://doi.org/10.1073/pnas.1209018109
Pinske C, Sargent F, Sawers RG (2015) SlyD-dependent nickel delivery limits maturation of [NiFe]-hydrogenases in late-stationary phase Escherichia coli cells. Metallomics 7(4):683–690. https://doi.org/10.1039/c5mt00019j
Pompidor G, Maillard AP, Girard E, Gambarelli S, Kahn R, Coves J (2008) X-ray structure of the metal-sensor CnrX in both the apo- and copper-bound forms. FEBS Lett 582(28):3954–3958. https://doi.org/10.1016/j.febslet.2008.10.042
Proshkin S, Rahmouni AR, Mironov A, Nudler E (2010) Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328(5977):504–508. https://doi.org/10.1126/science.1184939
Quaranta D, McEvoy MM, Rensing C (2009) Site-directed mutagenesis identifies a molecular switch involved in copper sensing by the histidine kinase CinS in Pseudomonas putida KT2440. J Bacteriol 191(16):5304–5311. https://doi.org/10.1128/jb.00551-09
Ranquet C, Ollagnier-de-Choudens S, Loiseau L, Barras F, Fontecave M (2007) Cobalt stress in Escherichia coli. J Biol Chem 282:30442–30451
Reith F, Rogers SL, McPhail DC, Webb D (2006) Biomineralization of gold: biofilms on bacterioform gold. Science 313:233–236
Reith F, Lengke MF, Falconer D, Craw D, Southam G (2007) The geomicrobiology of gold. ISME J 1:567–584
Ren J, Kotaka M, Lockyer M, Lamb HK, Hawkins AR, Stammers DK (2005) GTP cyclohydrolase II structure and mechanism. J Biol Chem 280(44):36912–36919. https://doi.org/10.1074/jbc.M507725200
Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27(2–3):197–213. https://doi.org/10.1016/S0168-6445(03)00049-4
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
Rey L, Imperial J, Palacios JM, Ruizargueso T (1994) Purification of Rhizobium leguminosarum HypB, a nickel-binding protein required for hydrogenase synthesis. J Bacteriol 176(19):6066–6073. https://doi.org/10.1128/jb.176.19.6066-6073.1994
Rice AJ, Park A, Pinkett HW (2014) Diversity in ABC transporters: Type I, II and III importers. Crit Rev Biochem Mol Biol 49(5):426–437. https://doi.org/10.3109/10409238.2014.953626
Rouviere PE, De Las PA, Mecsas J, Lu CZ, Rudd KE, Gross CA (1995) rpoE, the gene encoding the second heat-shock sigma factor, sigma E in Escherichia coli. Embo J 14(5):1032–1042
Roux M, Coves J (2002) The iron-containing superoxide dismutase of Ralstonia metallidurans CH34. FEMS Microbiol Lett 210(1):129–133
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 11:841–847
Sankar P, Lee JH, Shanmugam KT (1985) Cloning of hydrogenase genes and fine-structure analysis of an operon essential for H2 metabolism in Escherichia coli. J Bacteriol 162(1):353–360
Sankaran B, Bonnett SA, Shah K, Gabriel S, Reddy R, Schimmel P, Rodionov DA, de Crécy-Lagard V, Helmann JD, Iwata-Reuyl D, Swairjo MA (2009) Zinc-independent folate biosynthesis: genetic, biochemical, and structural investigations reveal new metal dependence for GTP cyclohydrolase IB. J Bacteriol 191:6936–6949
Sarkar P, Sardesai AA, Murakami KS, Chatterji D (2013) Inactivation of the bacterial RNA polymerase due to acquisition of secondary structure by the omega subunit. J Biol Chem 288(35):25076–25087. https://doi.org/10.1074/jbc.M113.468520
Schauer K, Gouget B, Carriere M, Labigne A, de Reuse H (2007) Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol 63(4):1054–1068
Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Trends Biochem Sci 33(7):330–338
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. https://doi.org/10.1111/j.1365-2958.2009.06792.x
Schmidt C, Schwarzenberger C, Grosse C, Nies DH (2014) FurC regulates expression of zupT for the central zinc importer ZupT of Cupriavidus metallidurans. J Bacteriol 196:3461–3471
Schulte M, Blake D, Hoehler T, McCollom T (2006) Serpentinization and its implications for life on the early Earth and Mars. Astrobiology 6(2):364–376. https://doi.org/10.1089/ast.2006.6.364
Schulz V, Schmidt-Vogler C, Strohmeyer P, Weber S, Kleemann D, Nies DH, Herzberg M (2021) Behind the shield of Czc: ZntR controls expression of the gene for the zinc-exporting P-type ATPase ZntA in Cupriavidus metallidurans. J Bacteriol 203(11):e00052–e00021
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
Shin JH, Oh SY, Kim SJ, Roe JH (2007) The zinc-responsive regulator Zur controls a zinc uptake system and some ribosomal proteins in Streptomyces coelicolor A3(2). J Bacteriol 189(11):4070–4077
Siche S, Neubauer O, Hebbeln P, Eitinger T (2010) A bipartite S unit of an ECF-type cobalt transporter. Res Microbiol 161(10):824–829. https://doi.org/10.1016/j.resmic.2010.09.010
Sleep NH, Meibom A, Fridriksson T, Coleman RG, Bird DK (2004) H2-rich fluids from serpentinization: geochemical and biotic implications. Proc Natl Acad Sci U S A 101:12818–12823
Spitzer J (2011) From water and ions to crowded biomacromolecules: in vivo structuring of a prokaryotic cell. Microbiol Mol Biol R 75(3):491–506. https://doi.org/10.1128/Mmbr.00010-11
Spitzer J, Poolman B (2009) The role of biomacromolecular crowding, ionic strength, and physicochemical gradients in the complexities of life’s emergence. Microbiol Mol Biol Rev 73(2):371–388. https://doi.org/10.1128/mmbr.00010-09
Staron A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, Mascher T (2009) The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol Microbiol 74(3):557–581. https://doi.org/10.1111/j.1365-2958.2009.06870.x
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 470:558–563. https://doi.org/10.1038/nature09743
Svetlov V, Nudler E (2013) Basic mechanism of transcription by RNA polymerase II. Biochim Biophys Acta 1829(1):20–28. https://doi.org/10.1016/j.bbagrm.2012.08.009
Sydor AM, Liu J, Zamble DB (2011) Effects of metal on the biochemical properties of Helicobacter pylori HypB, a maturation factor of [NiFe]-hydrogenase and urease. J Bacteriol 193(6):1359–1368. https://doi.org/10.1128/jb.01333-10
Sydor AM, Jost M, Ryan KS, Turo KE, Douglas CD, Drennan CL, Zamble DB (2013) Metal binding properties of Escherichia coli YjiA, a member of the metal homeostasis-associated COG0523 family of GTPases. Biochemist 52(10):1788–1801. https://doi.org/10.1021/Bi301600z
Sydor AM, Lebrette H, Ariyakumaran R, Cavazza C, Zamble DB (2014) Relationship between Ni(II) and Zn(II) coordination and nucleotide binding by the Helicobacter pylori [NiFe]-hydrogenase and urease maturation factor HypB. J Biol Chem 289(7):3828–3841. https://doi.org/10.1074/jbc.M113.502781
Tan KM, Sather A, Robertson JL, Moy S, Roux B, Joachimiak A (2009) Structure and electrostatic property of cytoplasmic domain of ZntB transporter. Protein Sci 18(10):2043–2052. https://doi.org/10.1002/pro.215
Taudte N, Grass G (2010) Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli. Biometals 23(4):643–656. https://doi.org/10.1007/s10534-010-9319-z
Thieme D, Neubauer P, Nies DH, Grass G (2008) Sandwich hybridization assay for sensitive detection of dynamic changes in mRNA transcript levels in crude Escherichia coli cell extracts in response to copper ions. Appl Environ Microbiol 74(24):7463–7470. https://doi.org/10.1128/aem.01370-08
Thorgersen MP, Downs DM (2007) Cobalt targets multiple metabolic processes in Salmonella enterica. J Bacteriol 189:7774–7781
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
Tottey S, Harvie DR, Robinson NJ (2007) Understanding how cells allocate metals. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals, Microbiology monographs, vol 6. Springer-Verlag, Berlin, pp 3–36
Trepreau J, Girard E, Maillard AP, de Rosny E, Petit-Haertlein I, Kahn R, Coves J (2011) Structural basis for metal sensing by CnrX. J Mol Biol 408(4):766–779. https://doi.org/10.1016/j.jmb.2011.03.014
Trepreau J, Grosse C, Mouesca J-M, Sarret G, Girard E, Petit-Hartlein 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 6:263–273
Tseng T-T, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MHJ (1999) The RND superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1:107–125
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 23:493–503
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. Antonie Van Leeuwenhoek 96(2):205–226. https://doi.org/10.1007/s10482-009-9345-4
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 Genomics 13:111. https://doi.org/10.1186/1471-2164-13-111
Van Houdt R, Provoost A, Van Assche A, Leys N, Lievens B, Mijnendonckx K, Monsieurs P (2018) Cupriavidus metallidurans strains with different mobilomes and from distinct environments have comparable phenomes. Genes-Basel 9(10):ARTN 507. https://doi.org/10.3390/genes9100507
Verstraeten N, Fauvart M, Versees W, Michiels J (2011) The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75(3):507–542. https://doi.org/10.1128/MMBR.00009-11
Volentini SI, Farias RN, Rodriguez-Montelongo L, Rapisarda VA (2011) Cu(II)-reduction by Escherichia coli cells is dependent on respiratory chain components. Biometals 24(5):827–835. https://doi.org/10.1007/s10534-011-9436-3
von Rozycki T, Nies DH (2009) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96:115–139
von Rozycki T, Nies DH, Saier MHJ (2005) Genomic analyses of transport proteins in Ralstonia metallidurans. Comp Func Genom 6:17–56
Walderhaug M, Polarek J, Voelkner P, Daniel J, Hesse J, Altendorf K, Epstein W (1992) KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J Bacteriol 174:2152–2159
Waldron KJ, Rutherford JC, Ford D, Robinson NJ (2009) Metalloproteins and metal sensing. Nature 460(7257):823–830. https://doi.org/10.1038/nature08300
Wan Q, Ahmad MF, Fairman J, Gorzelle B, de la Fuente M, Dealwis C, Maguire ME (2011) X-ray crystallography and isothermal titration calorimetry studies of the Salmonella zinc transporter ZntB. Structure 19(5):700–710. https://doi.org/10.1016/j.str.2011.02.011
Watanabe S, Kawashima T, Nishitani Y, Kanai T, Wada T, Inaba K, Atomi H, Imanaka T, Miki K (2015) Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancer. Proc Natl Acad Sci U S A 112(25):7701–7706. https://doi.org/10.1073/pnas.1503102112
Weast RC (1984) CRC handbook of chemistry and physics, 64th edn. CRC Press, Boca Raton, FL
Wei YN, 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
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 195:2298–2308. https://doi.org/10.1128/JB.01951-12
Wiesemann N, Bütof L, Herzberg M, Hause G, Berthold L, Etschmann B, Brugger J, Martinéz-Criado G, Dobritzsch D, Baginski S, Reith F, Nies DH (2017) Synergistic toxicity of copper and gold compounds in Cupriavidus metallidurans. Appl Environ Microbiol 83(23):e01679–e01617. https://doi.org/10.1128/AEM.01679-17
Williams JR, Morgan AG, Rouch DA, Brown NL, Lee BTO (1993) Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. Appl Environ Microbiol 59(8):2531–2537
Wilson TH, Ding PZ (2001) Sodium-substrate cotransport in bacteria. Biochim Biophys Acta 1505(1):121–130
Wolfram L, Eitinger T, Friedrich B (1991) Construction and properties of a triprotein containing the high-affinity nickel transporter of Alcaligenes eutrophus. FEBS Lett 283(1):109–112
Worlock AJ, Smith RL (2002) ZntB is a novel Zn2+ transporter in Salmonella enterica serovar typhimurium. J Bacteriol 184(16):4369–4373
Wu FYH, Huang WJ, Sinclair RB, Powers L (1992) The structure of the zinc sites of Escherichia coli DNA-dependent RNA polymerase. J Biol Chem 267(35):25560–25567
**a W, Li HY, Sze KH, Sun HZ (2009) Structure of a nickel chaperone, HypA, from Helicobacter pylori reveals two distinct metal binding sites. J Amer Chem Soc 131(29):10031–10040. https://doi.org/10.1021/ja900543y
**a W, Li HY, Yang XM, Wong KB, Sun HZ (2012) Metallo-GTPase HypB from Helicobacter pylori and its interaction with nickel chaperone protein HypA. J Biol Chem 287(9):6753–6763. https://doi.org/10.1074/jbc.M111.287581
Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280(2):1448–1456. https://doi.org/10.1074/jbc.M410104200
Yang XM, Li HY, Cheng TF, **a W, Lai YT, Sun HZ (2014) Nickel translocation between metallochaperones HypA and UreE in Helicobacter pylori. Metallomics 6(9):1731–1736. https://doi.org/10.1039/c4mt00134f
Yang X, Li H, Lai TP, Sun H (2015) UreE-UreG complex facilitates nickel transfer and preactivates GTPase of UreG in Helicobacter pylori. J Biol Chem 290(20):12474–12485. https://doi.org/10.1074/jbc.M114.632364
Yuen MH, Fong YH, Nim YS, Lau PH, Wong KB (2017) Structural insights into how GTP-dependent conformational changes in a metallochaperone UreG facilitate urease maturation. Proc Natl Acad Sci U S A 114(51):E10890–E10898. https://doi.org/10.1073/pnas.1712658114
Zambelli B, Banaszak K, Merloni A, Kiliszek A, Rypniewski W, Ciurli S (2013) Selectivity of Ni(II) and Zn(II) binding to Sporosarcina pasteurii UreE, a metallochaperone in the urease assembly: a calorimetric and crystallographic study. J Biol Inorg Chem 18(8):1005–1017. https://doi.org/10.1007/s00775-013-1049-6
Zambelli B, Berardi A, Martin-Diaconescu V, Mazzei L, Musiani F, Maroney MJ, Ciurli S (2014) Nickel binding properties of Helicobacter pylori UreF, an accessory protein in the nickel-based activation of urease. J Biol Inorg Chem 19(3):319–334. https://doi.org/10.1007/s00775-013-1068-3
Ziani W, Maillard AP, Petit-Hartlein I, Garnier N, Crouzy S, Girard E, Coves J (2014) The X-ray structure of NccX from Cupriavidus metallidurans 31A illustrates potential dangers of detergent solubilization when generating and interpreting crystal structures of membrane proteins. J Biol Chem 289(45):31160–31172. https://doi.org/10.1074/jbc.M114.586537
Zilberstein D, Agmon V, Schuldiner S, Padan E (1984) Escherichia coli intracellilar pH, membrane potential, and cell growth. J Bacteriol 158:246–252
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Nies, D.H. (2022). How is a Zinc Ion Correctly Allocated to a Zinc-dependent Protein?. In: Hurst, C.J. (eds) Microbial Metabolism of Metals and Metalloids. Advances in Environmental Microbiology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-97185-4_19
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