Abstract
ABSTRACT The transition metals nickel and cobalt, essential components of many enzymes, are taken up by specific transport systems of several different types. We integrated in silico and in vivo methods for the analysis of various protein families containing both nickel and cobalt transport systems in prokaryotes. For functional annotation of genes, we used two comparative genomic approaches: identification of regulatory signals and analysis of the genomic positions of genes encoding candidate nickel/cobalt transporters. The nickel-responsive repressor NikR regulates many nickel uptake systems, though the NikR-binding signal is divergent in various taxonomic groups of bacteria and archaea. B 12 riboswitches regulate most of the candidate cobalt transporters in bacteria. The nickel/cobalt transporter genes are often colocalized with genes for nickel-dependent or coenzyme B 12 biosynthesis enzymes. Nickel/cobalt transporters of different families, including the previously known NiCoT, UreH, and HupE/UreJ families of secondary systems and the NikABCDE ABC-type transporters, showed a mosaic distribution in prokaryotic genomes. In silico analyses identified CbiMNQO and NikMNQO as the most widespread groups of microbial transporters for cobalt and nickel ions. These unusual uptake systems contain an ABC protein (CbiO or NikO) but lack an extracytoplasmic solute-binding protein. Experimental analysis confirmed metal transport activity for three members of this family and demonstrated significant activity for a basic module (CbiMN) of the Salmonella enterica serovar Typhimurium transporter.
References
54
Referenced
252
-
Abouhamad, W. N., M. Manson, M. M. Gibson, and C. F. Higgins. 1991. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol.5:1035-1047.
(
10.1111/j.1365-2958.1991.tb01876.x
) / Mol. Microbiol. (1991) -
Altschul, S. F., and E. V. Koonin. 1998. Iterated profile searches with PSI-BLAST—a tool for discovery in protein databases. Trends Biochem. Sci.23:444-447.
(
10.1016/S0968-0004(98)01298-5
) / Trends Biochem. Sci. (1998) - Baginsky, C., J. M. Palacios, J. Imperial, T. Ruiz-Argueso, and B. Brito. 2004. Molecular and functional characterization of the Azorhizobium caulinodans ORS571 hydrogenase gene cluster. FEMS Microbiol. Lett.237:399-405. / FEMS Microbiol. Lett. (2004)
10.1016/j.jmb.2004.05.028
-
Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and D. L. Wheeler. 2005. GenBank. Nucleic Acids Res.33:D34-D38.
(
10.1093/nar/gni032
) / Nucleic Acids Res. (2005) -
Bloom, S. L., and D. B. Zamble. 2004. Metal-selective DNA-binding response of Escherichia coli NikR. Biochemistry43:10029-10038.
(
10.1021/bi049404k
) / Biochemistry (2004) 10.1128/JB.183.4.1242-1247.2001
-
Burne, R. A., and Y. Y. Chen. 2000. Bacterial ureases in infectious diseases. Microbes Infect.2:533-542.
(
10.1016/S1286-4579(00)00312-9
) / Microbes Infect. (2000) 10.1128/JB.185.23.6773-6779.2003
-
Cherrier, M. V., L. Martin, C. Cavazza, L. Jacquamet, D. Lemaire, J. Gaillard, and J. C. Fontecilla-Camps. 2005. Crystallographic and spectroscopic evidence for high affinity binding of FeEDTA(H2O)- to the periplasmic nickel transporter NikA. J. Am. Chem. Soc.127:10075-10082.
(
10.1021/ja0518530
) / J. Am. Chem. Soc. (2005) -
Chivers, P. T., and R. T. Sauer. 2000. Regulation of high affinity nickel uptake in bacteria. Ni2+-dependent interaction of NikR with wild-type and mutant operator sites. J. Biol. Chem.275:19735-19741.
(
10.1074/jbc.M002232200
) / J. Biol. Chem. (2000) -
Chivers, P. T., and R. T. Sauer. 2002. NikR repressor: high-affinity nickel binding to the C-terminal domain regulates binding to operator DNA. Chem. Biol.9:1141-1148.
(
10.1016/S1074-5521(02)00241-7
) / Chem. Biol. (2002) -
Chivers, P. T., and T. H. Tahirov. 2005. Structure of Pyrococcus horikoshii NikR: nickel sensing and implications for the regulation of DNA recognition. J. Mol. Biol.348:597-607.
(
10.1016/j.jmb.2005.03.017
) / J. Mol. Biol. (2005) -
Contreras, M., J. M. Thiberge, M. A. Mandrand-Berthelot, and A. Labigne. 2003. Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol. Microbiol.49:947-963.
(
10.1046/j.1365-2958.2003.03621.x
) / Mol. Microbiol. (2003) 10.1101/gr.849004
-
Davidson, A. L., and J. Chen. 2004. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem.73:241-268.
(
10.1146/annurev.biochem.73.011303.073626
) / Annu. Rev. Biochem. (2004) 10.1128/JB.184.13.3569-3577.2002
-
Degen, O., M. Kobayashi, S. Shimizu, and T. Eitinger. 1999. Selective transport of divalent cations by transition metal permeases: the Alcaligenes eutrophus HoxN and the Rhodococcus rhodochrous NhlF. Arch. Microbiol.171:139-145.
(
10.1007/s002030050691
) / Arch. Microbiol. (1999) 10.1128/JB.181.2.670-674.1999
10.1128/jb.148.2.459-464.1981
-
Doukov, T. I., T. M. Iverson, J. Seravalli, S. W. Ragsdale, and C. L. Drennan. 2002. A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Science298:567-572.
(
10.1126/science.1075843
) / Science (2002) 10.1128/JB.186.22.7821-7825.2004
-
Eitinger, T., O. Degen, U. Böhnke, and M. Müller. 2000. Nic1p, a relative of bacterial transition metal permeases in Schizosaccharomyces pombe, provides nickel ion for urease biosynthesis. J. Biol. Chem.275:18029-18033.
(
10.1074/jbc.M001978200
) / J. Biol. Chem. (2000) -
Eitinger, T., J. Suhr, J. Moore, and J. A. C. Smith. 2005. Secondary transporters for nickel and cobalt ions: theme and variations. BioMetals18:399-405.
(
10.1007/s10534-005-3714-x
) / BioMetals (2005) -
Eitinger, T., L. Wolfram, O. Degen, and C. Anthon. 1997. A Ni2+ binding motif is the basis of high affinity transport of the Alcaligenes eutrophus nickel permease. J. Biol. Chem.272:17139-17144.
(
10.1074/jbc.272.27.17139
) / J. Biol. Chem. (1997) -
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol.17:368-376.
(
10.1007/BF01734359
) / J. Mol. Evol. (1981) -
Gelfand, M. S., E. V. Koonin, and A. A. Mironov. 2000. Prediction of transcription regulatory sites in Archaea by a comparative genomic approach. Nucleic Acids Res.28:695-705.
(
10.1093/nar/28.3.695
) / Nucleic Acids Res. (2000) -
Guillén-Navarro, K., G. Araíza, A. García-de Los Santos, Y. Mora, and M. F. Dunn. 2005. The Rhizobium etli bioMNY operon is involved in biotin transport. FEMS Microbiol. Lett.250:209-219.
(
10.1016/j.femsle.2005.07.020
) / FEMS Microbiol. Lett. (2005) 10.1128/JB.186.9.2520-2522.2004
-
Hebbeln, P., and T. Eitinger. 2004. Heterologous production and characterization of bacterial nickel/cobalt permeases. FEMS Microbiol. Lett.230:129-135.
(
10.1016/S0378-1097(03)00885-1
) / FEMS Microbiol. Lett. (2004) -
Heddle, J., D. J. Scott, S. Unzai, S. Y. Park, and J. R. Tame. 2003. Crystal structures of the liganded and unliganded nickel-binding protein NikA from Escherichia coli. J. Biol. Chem.278:50322-50329.
(
10.1074/jbc.M307941200
) / J. Biol. Chem. (2003) -
Hidalgo, E., J. M. Palacios, J. Murillo, and T. Ruiz-Argüeso. 1992. Nucleotide sequence and characterization of four additional genes of the hydrogenase structural operon from Rhizobium leguminosarum bv. viciae. J. Bacteriol.174:4130-4139.
(
10.1128/jb.174.12.4130-4139.1992
) / viciae. J. Bacteriol. (1992) 10.1128/JB.183.2.426-434.2001
10.1128/JB.186.9.2532-2539.2004
10.1128/jb.179.7.2259-2266.1997
-
Kobayashi, M., and S. Shimizu. 1999. Cobalt proteins. Eur. J. Biochem.261:1-9.
(
10.1046/j.1432-1327.1999.00186.x
) / Eur. J. Biochem. (1999) -
Levdikov, V. M., E. V. Blagova, J. A. Brannigan, L. Wright, A. A. Vagin, and A. J. Wilkinson. 2005. The structure of the oligopeptide-binding protein, AppA, from Bacillus subtilis in complex with a nonapeptide. J. Mol. Biol.345:879-892.
(
10.1016/j.jmb.2004.10.089
) / J. Mol. Biol. (2005) 10.1128/jb.176.2.432-442.1994
-
McMillan, D. J., M. Mau, and M. J. Walker. 1998. Characterisation of the urease gene cluster in Bordetella bronchiseptica. Gene208:243-251.
(
10.1016/S0378-1119(97)00651-3
) / Gene (1998) 10.1007/BF02759643
-
Mulrooney, S. B., and R. P. Hausinger. 2003. Nickel uptake and utilization by microorganisms. FEMS Microbiol. Rev.27:239-261.
(
10.1016/S0168-6445(03)00042-1
) / FEMS Microbiol. Rev. (2003) -
Nahvi, A., J. E. Barrick, and R. R. Breaker. 2004. Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. Nucleic Acids Res.32:143-150.
(
10.1093/nar/gkh167
) / Nucleic Acids Res. (2004) -
Navarro, C., L. F. Wu, and M. A. Mandrand-Berthelot. 1993. The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol. Microbiol.9:1181-1191.
(
10.1111/j.1365-2958.1993.tb01247.x
) / Mol. Microbiol. (1993) -
Overbeek, R., T. Begley, R. Butler, J. Choudhuri, H. Chuang, M. Cohoon, V. de Crécy-Lagard, N. Diaz, T. Disz, R. Edwards, M. Fonstein, E. D. Frank, S. Gerdes, E. Glass, A. Goesmann, A. Hanson, D. Iwata-Reuyl, R. Jensen, N. Jamshidi, L. Krause, M. Kubal, N. Larsen, B. Linke, A. C. McHardy, F. Meyer, H. Neuweger, G. Olsen, R. Olson, A. Osterman, V. Portnoy, G. Pusch, D. A. Rodionov, C. Rückert, J. Steiner, R. Stevens, I. Thiele, O. Vassieva, Y. Ye, O. Zagnitko, and V. Vonstein. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1,000 genomes. Nucleic Acids Res.33:5691-5702.
(
10.1093/nar/gki866
) / Nucleic Acids Res. (2005) -
Rodionov, D. A., I. Dubchak, A. Arkin, E. Alm, and M. S. Gelfand. 22 October 2004, posting date. Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Genome Biol.5:R90. [Online.] http://genomebiology.com/2004/5/11/R90 .
(
10.1186/gb-2004-5-11-r90
) / Genome Biol. 10.1074/jbc.M305837200
10.1128/jb.175.11.3303-3316.1993
-
Schreiter, E. R., M. D. Sintchak, Y. Guo, P. T. Chivers, R. T. Sauer, and C. L. Drennan. 2003. Crystal structure of the nickel-responsive transcription factor NikR. Nat. Struct. Biol.10:794-799.
(
10.1038/nsb985
) / Nat. Struct. Biol. (2003) 10.1128/JB.184.20.5706-5713.2002
-
Sukdeo, N., S. L. Clugston, E. Daub, and J. F. Honek. 2004. Distinct classes of glyoxalase I: metal specificity of the Yersinia pestis, Pseudomonas aeruginosa and Neisseria meningitidis enzymes. Biochem. J.384:111-117.
(
10.1042/BJ20041006
) / Biochem. J. (2004) 10.1093/nar/28.1.33
10.1093/nar/25.24.4876
-
Venter, H., R. A. Shilling, S. Velamakanni, L. Balakrishnan, and H. W. van Veen. 2003. An ABC transporter with a secondary-active multidrug translocator domain. Nature426:866-870.
(
10.1038/nature02173
) / Nature (2003) 10.1128/jb.177.7.1840-1843.1995
Dates
Type | When |
---|---|
Created | 19 years, 8 months ago (Dec. 13, 2005, 5:38 p.m.) |
Deposited | 4 years, 1 month ago (July 29, 2021, 1:28 p.m.) |
Indexed | 5 days, 17 hours ago (Aug. 31, 2025, 6:34 a.m.) |
Issued | 19 years, 8 months ago (Jan. 1, 2006) |
Published | 19 years, 8 months ago (Jan. 1, 2006) |
Published Print | 19 years, 8 months ago (Jan. 1, 2006) |
@article{Rodionov_2006, title={Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters}, volume={188}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.188.1.317-327.2006}, DOI={10.1128/jb.188.1.317-327.2006}, number={1}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Rodionov, Dmitry A. and Hebbeln, Peter and Gelfand, Mikhail S. and Eitinger, Thomas}, year={2006}, month=jan, pages={317–327} }