Skip to main content
SpringerLink
Log in

Tellurite resistance gene trgB confers copper tolerance to Rhodobacter capsulatus

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

To identify copper homeostasis genes in Rhodobacter capsulatus, we performed random transposon Tn5 mutagenesis. Screening of more than 10,000 Tn5 mutants identified tellurite resistance gene trgB as a so far unrecognized major copper tolerance determinant. The trgB gene is flanked by tellurite resistance gene trgA and cysteine synthase gene cysK2. While growth of trgA mutants was only moderately restricted by tellurite, trgB and cysK2 mutants were severely affected by tellurite, which implies that viability under tellurite stress requires increased cysteine levels. Mutational analyses revealed that trgB was the only gene in this chromosomal region conferring cross-tolerance towards copper. Expression of the monocistronic trgB gene required promoter elements overlapping the trgA coding region as shown by nested deletions. Neither copper nor tellurite affected trgB transcription as demonstrated by reverse transcriptase PCR and trgB–lacZ fusions. Addition of tellurite or copper gave rise to increased cellular tellurium and copper concentrations, respectively, as determined by inductively coupled plasma-optical emission spectroscopy. By contrast, cellular iron concentrations remained fairly constant irrespective of tellurite or copper addition. This is the first study demonstrating a direct link between copper and tellurite response in bacteria.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Achard ME, Tree JJ, Holden JA, Simpfendorfer KR, Wijburg OL, Strugnell RA, Schembri MA, Sweet MJ, Jennings MP, McEwan AG (2010) The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect Immun 78:2312–2319. doi:10.1128/IAI.01208-09

    Article  PubMed  CAS  Google Scholar 

  • Alcaraz LA, Gómez J, Ramírez P, Calvente JJ, Andreu R, Donaire A (2007) Folding and unfolding in the blue copper protein rusticyanin: role of the oxidation state. Bioinorg Chem Appl 2007:54232. doi:10.1155/2007/54232

    Article  Google Scholar 

  • Alexeyev MF (1995) Three kanamycin resistance gene cassettes with different polylinkers. Biotechniques 18:52–55

    PubMed  CAS  Google Scholar 

  • Andreini C, Banci L, Bestini I, Rosato A (2008) Occurrence of copper proteins through the three domains of life: a bioinformatic approach. J Proteome Res 7:209–216. doi:10.1021/pr070480u

    Article  PubMed  CAS  Google Scholar 

  • Avazéri C, Turner RJ, Pommier J, Weiner JH, Giordano G, Verméglio A (1997) Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite. Microbiology 143:1181–1189. doi:10.1099/00221287-143-4-1181

    Article  PubMed  Google Scholar 

  • Ba LA, Döring M, Jamier V, Jacob C (2010) Tellurium: an element with great biological potency and potential. Org Biomol Chem 8:4203–4216. doi:10.1039/C0OB00086H

    Article  PubMed  CAS  Google Scholar 

  • Banci L, Bertini I, Cantini F, Ciofi-Baffoni S (2010) Cellular copper distribution: a mechanistic systems biology approach. Cell Mol Life Sci 67:2563–2589. doi:10.1007/s00018-010-0330-x

    Article  PubMed  CAS  Google Scholar 

  • Borghese R, Zannoni D (2010) Acetate permease (ActP) is responsible for tellurite (TeO3 2−) uptake and resistance in cells of the facultative phototroph Rhodobacter capsulatus. Appl Environ Microbiol 76:942–944. doi:10.1128/AEM.02765-09

    Article  PubMed  CAS  Google Scholar 

  • Borsetti F, Borghese R, Francia F, Randi MR, Fedi S, Zannoni D (2003) Reduction of potassium tellurite to elemental tellurium and its effect on the plasma membrane redox components of the facultative phototroph Rhodobacter capsulatus. Protoplasma 221:153–161. doi:10.1007/s00709-002-0058-z

    Article  PubMed  CAS  Google Scholar 

  • Calderón IL, Arenas FA, Pérez JM, Fuentes DE, Araya MA, Saavedra CP, Tantaleán JC, Pichuantes SE, Youderian PA, Vásquez CC (2006) Catalases are NAD(P)H-dependent tellurite reductases. PLoS One 1:e70. doi:10.1371/journal.pone.0000070

    Article  PubMed  Google Scholar 

  • Calderón IL, Elías AO, Fuentes EL, Pradenas GA, Castro ME, Arenas FA, Pérez JM, Vásquez CC (2009) Tellurite-mediated disabling of [4Fe–4S] clusters of Escherichia coli dehydratases. Microbiology 155:1840–1846. doi:10.1099/mic.0.026260-0

    Article  PubMed  Google Scholar 

  • Castro ME, Molina R, Díaz W, Pichuantes SE, Vásquez CC (2008) The dihydrolipoamide dehydrogenase of Aeromonas caviae ST exhibits NADH-dependent tellurite reductase activity. Biochem Biophys Res Commun 375:91–94. doi:10.1016/j.bbrc.2008.07.119

    Article  PubMed  CAS  Google Scholar 

  • Chakravarthi S, Jessop CE, Bulleid NJ (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep 7:271–275. doi:10.1038/sj.embor.7400645

    Article  PubMed  CAS  Google Scholar 

  • Chasteen TG, Fuentes DE, Tantaleán JC, Vásquez CC (2009) Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol Rev 33:820–832. doi:10.1111/j.1574-6976.2009.00177.x

    Article  PubMed  CAS  Google Scholar 

  • Chien CC, Jiang MH, Tsai MR, Chien CC (2011) Isolation and characterization of an environmental cadmium- and tellurite-resistant Pseudomonas strain. Environ Toxicol Chem 30:2202–2207. doi:10.1002/etc.620

    Article  PubMed  CAS  Google Scholar 

  • Chillappagari S, Seubert A, Trip H, Kuipers OP, Marahiel MA, Miethke M (2010) Copper stress affects iron homeostasis by destabilizing iron–sulfur cluster formation in Bacillus subtilis. J Bacteriol 192:2512–2524. doi:10.1128/JB.00058-10

    Article  PubMed  CAS  Google Scholar 

  • Cunha RL, Gouvea IE, Juliano L (2009) A glimpse on biological activities of tellurium compounds. An Acad Bras Cienc 81:393–407. doi:10.1590/S0001-37652009000300006

    Article  PubMed  CAS  Google Scholar 

  • Drepper T, Wiethaus J, Giaourakis D, Gross S, Schubert B, Vogt M, Wiencek Y, McEwan AG, Masepohl B (2006) Cross-talk towards the response regulator NtrC controlling nitrogen metabolism in Rhodobacter capsulatus. FEMS Microbiol Lett 258:250–256. doi:10.1111/j.1574-6968.2006.00228.x

    Article  PubMed  CAS  Google Scholar 

  • Dunn CA, O’Handley SF, Frick DN, Bessman MJ (1999) Studies on the ADP-ribose pyrophosphatase subfamily of the nudix hydrolases and tentative identification of trgB, a gene associated with tellurite resistance. J Biol Chem 274:32318–32324. doi:10.1074/jbc.274.45.32318

    Article  PubMed  CAS  Google Scholar 

  • Fan B, Rosen BP (2002) Biochemical characterization of CopA, the Escherichia coli Cu(I)-translocating P-type ATPase. J Biol Chem 277:46987–46992. doi:10.1074/jbc.M208490200

    Article  PubMed  CAS  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 185:3804–3812. doi:10.1128/JB.185.13.3804-3812.2003

    Article  PubMed  Google Scholar 

  • Gisin J, Müller A, Pfänder Y, Leimkühler S, Narberhaus F, Masepohl B (2010) A Rhodobacter capsulatus member of a universal permease family imports molybdate and other oxyanions. J Bacteriol 192:5943–5952. doi:10.1128/JB.00742-10

    Article  PubMed  CAS  Google Scholar 

  • Grass G, Thakali K, Klebba PE, Thieme D, Müller A, Wildner GF, Rensing C (2004) Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J Bacteriol 186:5826–5833. doi:10.1128/JB.186.17.5826-5833.2004

    Article  PubMed  CAS  Google Scholar 

  • Helbig K, Bleuel C, Krauss GJ, Nies DH (2008) Glutathione and transition-metal homeostasis in Escherichia coli. J Bacteriol 190:5431–5438. doi:10.1128/JB.00271-08

    Article  PubMed  CAS  Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418. doi:10.1146/annurev.micro.57.030502.090938

    Article  PubMed  CAS  Google Scholar 

  • Jacobson EL, Cervantes-Laurean D, Jacobson MK (1994) Glycation of proteins by ADP-ribose. Mol Cell Biochem 138:207–212. doi:10.1007/BF00928463

    Article  PubMed  CAS  Google Scholar 

  • Kershaw CJ, Brown NL, Constantinidou C, Patel MD, Hobman JL (2005) The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187–1198. doi:10.1099/mic.0.27650-0

    Article  PubMed  CAS  Google Scholar 

  • Klipp W, Masepohl B, Pühler A (1988) Identification and mapping of nitrogen fixation genes of Rhodobacter capsulatus: duplication of a nifA–nifB region. J Bacteriol 170:693–699

    PubMed  CAS  Google Scholar 

  • Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM II, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176. doi:10.1016/0378-1119(95)00584-1

    Article  PubMed  CAS  Google Scholar 

  • Leimkühler S, Kern M, Solomon PS, McEwan AG, Schwarz G, Mendel RR, Klipp W (1998) Xanthine dehydrogenase from the phototrophic purple bacterium Rhodobacter capsulatus is more similar to its eukaryotic counterparts than to prokaryotic molybdenum enzymes. Mol Microbiol 27:853–869. doi:10.1046/j.1365-2958.1998.00733.x

    Article  PubMed  Google Scholar 

  • Lloyd-Jones G, Osborn AM, Ritchie DA, Strike P, Hobman JL, Brown NL, Rouch DA (1994) Accumulation and intracellular fate of tellurite in tellurite-resistant Escherichia coli: a model for the mechanism of resistance. FEMS Microbiol Lett 118:113–119. doi:10.1111/j.1574-6968.1994.tb06812.x

    Article  PubMed  CAS  Google Scholar 

  • MacDonald LJ, Moss J (1994) Enzymatic and nonenzymatic ADP-ribosylation of cysteine. Mol Cell Biochem 138:221–226. doi:10.1007/BF00928465

    Article  Google Scholar 

  • Macomber L, Imlay JA (2009) The iron–sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 106:8344–8349. doi:10.1073/pnas.0812808106

    Article  PubMed  CAS  Google Scholar 

  • Magnani D, Solioz M (2007) How bacteria handle copper. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals. Springer, Heidelberg, pp 259–285. doi:10.1007/7171_2006_081

    Chapter  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229. doi:10.1093/nar/gkq1189

    Article  PubMed  Google Scholar 

  • Masepohl B, Hallenbeck PC (2010) Nitrogen and molybdenum control of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus. Adv Exp Med Biol 675:49–70. doi:10.1007/978-1-4419-1528-3_4

    Article  PubMed  CAS  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Moore MD, Kaplan S (1992) Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J Bacteriol 174:1505–1514

    PubMed  CAS  Google Scholar 

  • Nicolaisen K, Hahn A, Valdebenito M, Moslavac S, Samborski A, Maldener I, Wilken C, Valladares A, Flores E, Hantke K, Schleiff E (2010) The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta 1798:2131–2140. doi:10.1016/j.bbamem.2010.07.008

    Article  PubMed  CAS  Google Scholar 

  • O’Gara JP, Gomelsky M, Kaplan S (1997) Identification and molecular genetic analysis of multiple loci contributing to high-level tellurite resistance in Rhodobacter sphaeroides 2.4.1. Appl Environ Microbiol 63:4713–4720

    PubMed  Google Scholar 

  • Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57:289–301. doi:10.1111/j.1365-313X.2008.03686.x

    Article  PubMed  CAS  Google Scholar 

  • Onder O, Aygun-Sunar S, Selamoglu N, Daldal F (2010) A glimpse into the proteome of phototrophic bacterium Rhodobacter capsulatus. Adv Exp Med Biol 675:179–209. doi:10.1007/978-1-4419-1528-3_11

    Article  PubMed  CAS  Google Scholar 

  • Osman D, Cavet JS (2008) Copper homeostasis in bacteria. Adv Appl Microbiol 65:217–247. doi:10.1016/S0065-2164(08)00608-4

    Article  PubMed  CAS  Google Scholar 

  • Ottosson LG, Logg K, Ibstedt S, Sunnerhagen P, Käll M, Blomberg A, Warringer J (2010) Sulfate assimilation mediates tellurite reduction and toxicity in Saccharomyces cerevisiae. Eukaryot Cell 9:1635–1647. doi:10.1128/EC.00078-10

    Article  PubMed  CAS  Google Scholar 

  • 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 276:30670–30677. doi:10.1074/jbc.M104122200

    Article  PubMed  CAS  Google Scholar 

  • Pawlik G, Kulajta C, Sachelaru I, Schröder S, Waidner B, Hellwig P, Daldal F, Koch HG (2010) The putative assembly factor CcoH is stably associated with the cbb3-type cytochrome oxidase. J Bacteriol 192:6378–6389. doi:10.1128/JB.00988-10

    Article  PubMed  CAS  Google Scholar 

  • Pérez JM, Calderón IL, Arenas FA, Fuentes DE, Pradenas GA, Fuentes EL, Sandoval JM, Castro ME, Elías AO, Vásquez CC (2007) Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS One 2:e211. doi:10.1371/journal.pone.0000211

    Article  PubMed  Google Scholar 

  • Rademacher C, Moser R, Lackmann J-W, Klinkert B, Narberhaus F, Masepohl B (2012) Transcriptional and post-transcriptional events control copper-responsive expression of a Rhodobacter capsulatus multicopper oxidase. J Bacteriol 194:1849–1859. doi:10.1128/JB.06274-11

    Article  PubMed  CAS  Google Scholar 

  • Ramírez A, Castañeda M, Xiqui ML, Sosa A, Baca BE (2006) Identification, cloning and characterization of cysK, the gene encoding O-acetylserine (thiol)-lyase from Azospirillum brasilense, which is involved in tellurite resistance. FEMS Microbiol Lett 261:272–279. doi:10.1111/j.1574-6968.2006.00369.x

    Article  PubMed  Google Scholar 

  • Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213. doi:10.1016/S0168-6445(03)00049-4

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Jara A, Latorre M, López G, Bourgogne A, Murray BE, Cambiazo V, González M (2010) Genome-wide transcriptome analysis of the adaptive response of Enterococcus faecalis to copper exposure. Biometals 23:1105–1112. doi:10.1007/s10534-010-9356-7

    Article  PubMed  CAS  Google Scholar 

  • Rigobello MP, Folda A, Citta A, Scutari G, Gandin V, Fernandes AP, Rundlöf AK, Marzano C, Björnstedt M, Bindoli A (2011) Interaction of selenite and tellurite with thiol-dependent redox enzymes: kinetics and mitochondrial implications. Free Radic Biol Med 50:1620–1629. doi:10.1016/j.freeradbiomed.2011.03.006

    Article  PubMed  CAS  Google Scholar 

  • Robinson NJ (2011) Structural biology: a platform for copper pumps. Nature 475:41–42. doi:10.1038/475041a

    Article  PubMed  CAS  Google Scholar 

  • Silver S, Le Phung T (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 32:587–605. doi:10.1007/s10295-005-0019-6

    Article  PubMed  CAS  Google Scholar 

  • Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1:784–791. doi:10.1038/nbt1183-784

    Article  CAS  Google Scholar 

  • Singh SK, Grass G, Rensing C, Montfort WR (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186:7815–7817. doi:10.1128/JB.186.22.7815-7817.2004

    Article  PubMed  CAS  Google Scholar 

  • Singleton C, Le Brun NE (2009) The N-terminal soluble domains of Bacillus subtilis CopA exhibit a high affinity and capacity for Cu(I) ions. Dalton Trans 28:688–696. doi:10.1039/B810412C

    Article  Google Scholar 

  • Singleton C, Banci L, Ciofi-Baffoni S, Tenori L, Kihlken MA, Boetzel R, Le Brun NE (2008) Structure and Cu(I)-binding properties of the N-terminal soluble domains of Bacillus subtilis CopA. Biochem J 411:571–579. doi:10.1042/BJ20071620

    Article  PubMed  CAS  Google Scholar 

  • Solioz M, Stoyanov JV (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27:183–195. doi:10.1016/S0168-6445(03)00053-6

    Article  PubMed  CAS  Google Scholar 

  • Solioz M, Abicht HK, Mermod M, Mancini S (2010) Response of Gram-positive bacteria to copper stress. J Biol Inorg Chem 15:3–14. doi:10.1007/s00775-009-0588-3

    Article  PubMed  CAS  Google Scholar 

  • Strnad H, Lapidus A, Paces J, Ulbrich P, Vlcek C, Paces V, Haselkorn R (2010) Complete genome sequence of the photosynthetic purple nonsulfur bacterium Rhodobacter capsulatus SB 1003. J Bacteriol 192:3545–3546. doi:10.1128/JB.00366-10

    Article  PubMed  CAS  Google Scholar 

  • Su CC, Long F, Yu EW (2011) The Cus efflux system removes toxic ions via a methionine shuttle. Protein Sci 20:6–18. doi:10.1002/pro.532

    Article  PubMed  CAS  Google Scholar 

  • Taylor DE (1999) Bacterial tellurite resistance. Trends Microbiol 7:111–115. doi:10.1016/S0966-842X(99)01454-7

    Article  PubMed  CAS  Google Scholar 

  • Teitzel GM, Geddie A, De Long SK, Kirisits MJ, Whiteley M, Parsek MR (2006) Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J Bacteriol 188:7242–7256. doi:10.1128/JB.00837-06

    Article  PubMed  CAS  Google Scholar 

  • Tremaroli V, Fedi S, Zannoni D (2007) Evidence for a tellurite-dependent generation of reactive oxygen species and absence of a tellurite-mediated adaptive response to oxidative stress in cells of Pseudomonas pseudoalcaligenes KF707. Arch Microbiol 187:127–135. doi:10.1007/s00203-006-0179-4

    Article  PubMed  CAS  Google Scholar 

  • Turner RJ, Weiner J, Taylor DE (1999) Tellurite-mediated thiol oxidation in Escherichia coli. Microbiology 145:2549–2557

    PubMed  CAS  Google Scholar 

  • Turner RJ, Aharonowitz Y, Weiner JH, Taylor DE (2001) Glutathione is a target in tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli. Can J Microbiol 47:33–40. doi:10.1139/cjm-47-1-33

    PubMed  CAS  Google Scholar 

  • Urbański NK, Beresewicz A (2000) Generation of *OH initiated by interaction of Fe2+ and Cu+ with dioxygen; comparison with the Fenton chemistry. Acta Biochim Pol 47:951–962

    PubMed  Google Scholar 

  • Vásquez CC, Saavedra CP, Loyola CA, Araya MA, Pichuantes S (2001) The product of the cysK gene of Bacillus stearothermophilus V mediates potassium tellurite resistance in Escherichia coli. Curr Microbiol 43:418–423. doi:10.1007/s002840010331

    Article  PubMed  Google Scholar 

  • Vieira J, Messing J (1982) The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268. doi:10.1016/0378-119(82)90015-4

    Article  PubMed  CAS  Google Scholar 

  • Waldron KJ, Robinson NJ (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7:25–35. doi:10.1038/nrmicro2057

    Article  PubMed  CAS  Google Scholar 

  • Weaver PF, Wall JD, Gest H (1975) Characterization of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216. doi:10.1007/BF00447139

    Article  PubMed  CAS  Google Scholar 

  • Wiethaus J, Wildner GF, Masepohl B (2006) The multicopper oxidase CutO confers copper tolerance to Rhodobacter capsulatus. FEMS Microbiol Lett 256:67–74. doi:10.1111/j.1574-6968.2005.00094.x

    Article  PubMed  CAS  Google Scholar 

  • Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FSL (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608–1615. doi:10.1093/bioinformatics/btq249

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Grant Ma 1814/3-3 from the Deutsche Forschungsgemeinschaft.

Author information

Authors and Affiliations

  1. Biologie der Mikroorganismen, Fakultät für Biologie und Biotechnologie, Ruhr-Universität Bochum, 44780, Bochum, Germany

    Corinna Rademacher, Marie-Christine Hoffmann, Jan-Wilm Lackmann, Roman Moser, Yvonne Pfänder, Franz Narberhaus & Bernd Masepohl

  2. Molekulare Enzymologie, Institut für Biochemie und Biologie, Universität Potsdam, 14469, Potsdam, Germany

    Silke Leimkühler

Authors
  1. Corinna Rademacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Christine Hoffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan-Wilm Lackmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roman Moser
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yvonne Pfänder
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Silke Leimkühler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Franz Narberhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bernd Masepohl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Masepohl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rademacher, C., Hoffmann, MC., Lackmann, JW. et al. Tellurite resistance gene trgB confers copper tolerance to Rhodobacter capsulatus . Biometals 25, 995–1008 (2012). https://doi.org/10.1007/s10534-012-9566-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-012-9566-2

Keywords

Search

Navigation