Identification of the<i>nik</i>Gene Cluster of<i>Brucella suis</i>: Regulation and Contribution to Urease Activity

Jubier-Maurin, Véronique; Rodrigue, Agnès; Ouahrani‐Bettache, Safia; Layssac, Marion; Mandrand‐Berthelot, Marie‐Andrée; Köhler, Stephan; Liautard, Jean‐Pierre

doi:10.1128/jb.183.2.426-434.2001

Cited by 57 publications

(52 citation statements)

References 44 publications

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“…Though distantly related ABC transporter systems from pathogenic Yersinia pseudotuberculosis and Brucella suis are also implicated in the high-affinity nickel uptake (33,49), many other representatives of this ABC transporter family are involved in uptake of other compounds, i.e., dipeptides and oligopeptides (1,37).…”

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confidence: 99%

Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters

et al. 2006

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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.The transition metals nickel and cobalt are essential cofactors for a number of prokaryotic enzymes involved in a variety of metabolic processes (36,41). Among the known nickeldependent enzymes are urease (8), [NiFe] hydrogenase, carbon monoxide dehydrogenase (Ni-CODH) (35), acetyl-coenzyme A decarbonylase/synthase (21), superoxide dismutase SodN (22), methyl-coenzyme M reductase (20), and glyoxylase I (50). In contrast to the diverse roles of nickel in microbial metabolism, cobalt is mainly found in the corrin ring of coenzyme B 12 , a cofactor involved in methyl group transfer and in rearrangement reactions (36). Since in natural environments, soluble Ni 2ϩ and Co 2ϩ are usually present only in trace amounts, the synthesis of the respective metalloenzymes requires high-affinity uptake of metal ions. Until recently, two major types of microbial high-affinity nickel and cobalt transporters were known: ATP-binding cassette (ABC) systems and secondary permeases of the NiCoT family (reviewed in reference 24).The NikABCDE system of Escherichia coli belongs to the nickel/peptide/opine ABC transporter family and is composed of the periplasmic binding protein NikA, two integral membrane components (NikB and -C), and two ATPases (NikD and -E) (43). The molecular basis of selective high-affinity binding of Ni 2ϩ remains elusive, although crystal structures of E. coli NikA have been determined by two approaches (10, 31).The two studies uncovered that N...

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Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters

et al. 2006

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“…In general, two types of nickel-specific uptake systems have been identified so far: (i) the multiple-component ATP binding cassette system called Nik, which was thought for a long time to be unique to Escherichia coli (39), until homologous systems were identified and characterized in Brucella suis (17) and Vibrio parahaemolyticus (28); and (ii) the nickel-cobalt transporter family, comprising homologous single polypeptides in a variety of microorganisms (8,32)-Helicobacter pylori (25), Ralstonia eutropha (7), Bradyrhizobium japonicum (11), Rhodococcus rhodochrous (18), and the thermophilic Bacillus species strain TB-90 (21)-which have all been characterized biochemically, or at least physiologically. During database searches, related sequences have been identified in the genomes of Mycobacterium tuberculosis and Mycobacterium avium; Salmonella enterica serovar Paratyphi, Salmonella enterica serovar Typhi, and Salmonella enterica serovar Typhimurium; Staphylococcus aureus; Yersinia pestis; and the fission yeast Schizosaccharomyces pombe (8).…”

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Conserved Low-Affinity Nickel-Binding Amino Acids Are Essential for the Function of the Nickel Permease NixA of Helicobacter pylori

Wolfram

Bauerfeind

2002

J Bacteriol

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The transition metal nickel is an essential trace element of at least five biological processes (14, 31): (i) hydrolysis of urea, (ii) oxidation and evolution of molecular hydrogen, (iii) carbon monoxide dehydrogenase-mediated acetate metabolism under anaerobic conditions, (iv) reduction of methyl coenzyme M to methane, and (v) detoxification of superoxide anion radicals. Uptake of nickel is a prerequisite for those organisms which catalyze nickel-dependent reactions. Ni 2ϩ -the most prevalent form-is taken up by nonspecific Mg 2ϩ transport systems and high-affinity systems specific for the transport of nickel (see reference 8 for a review).In general, two types of nickel-specific uptake systems have been identified so far: (i) the multiple-component ATP binding cassette system called Nik, which was thought for a long time to be unique to Escherichia coli (39), until homologous systems were identified and characterized in Brucella suis (17) and Vibrio parahaemolyticus (28); and (ii) the nickel-cobalt transporter family, comprising homologous single polypeptides in a variety of microorganisms (8, 32)-Helicobacter pylori (25), Ralstonia eutropha (7), Bradyrhizobium japonicum (11), Rhodococcus rhodochrous (18), and the thermophilic Bacillus species strain TB-90 (21)-which have all been characterized biochemically, or at least physiologically. During database searches, related sequences have been identified in the genomes of Mycobacterium tuberculosis and Mycobacterium avium; Salmonella enterica serovar Paratyphi, Salmonella enterica serovar Typhi, and Salmonella enterica serovar Typhimurium; Staphylococcus aureus; Yersinia pestis; and the fission yeast Schizosaccharomyces pombe (8).Members of the second family share two recognition sequences within their common topology of eight transmembrane helices (TMs): NH 2 -Arg/Lys-His-Ala-Xaa-Asp-Ala-Asp-HisIle/Leu-COOH in TM II and NH 2 -Gly-(Xaa) 2 -Phe-(Xaa) 2 -Gly-His-Ser/Thr-Ser/Thr-Val/Ile-Val-COOH in TM III (32). Besides these two conserved motifs, 48 other conserved amino acids scattered through the protein could be detected after sequence alignment. Recently, two other motifs have been proposed (9): NH 2 -Leu-Gly-Xaa-Asp/Glu-Thr-Ala/Ser-Thr/ Ser-Glu-COOH in TM V and NH 2 -Gly-Met-(Xaa) 3 -Asp-Thr/ Ser-Xaa-Asp-COOH in TM VI.The high-affinity nickel transport protein NixA of the human pathogen H. pylori was discovered when a gene bank clone of strain ATCC 43504 was found to enhance the coexpressed urease activity in E. coli (25). The urease-an important virulence factor of H. pylori-is a major sink of nickel in this organism, representing up to 6% of the soluble cell protein (16). It converts urea to ammonia and carbamate, the latter decomposing spontaneously to carbon dioxide and ammonia. The released ammonia has been postulated to allow the survival of H. pylori and its colonization of the low-pH environment of the gastric mucosa, which causes Type B gastritis as well as gastric and duodenal ulceration (1,4,19,23,24). Persistent infection is strongly associated with...

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“…Like NikD and NikE, ORF4 (268 amino acids, molecular mass of 29,472 Da) and ORF5 (221 amino acids, molecular mass of 24,754 Da) possess characteristic ATP-binding domains (37), suggesting a role in coupling energy to the transport process. ORF1 to ORF5 also showed homology to the nikABCDE cluster of B. suis (24 to 32% identity) (18) and that of V. parahaemolyticus (33 to 41% identity) (26). They also share 34 to 43% identity with the dipeptide transport system encoded by the dpp operon from Streptococcus pyogenes (27).…”

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confidence: 82%

“…For the first time, we demonstrate the presence of two transporters specific for nickel in a prokaryote. The human and animal pathogen Y. pseudotuberculosis possesses (i) an ABC transporter encoded by the yntABCDE gene cluster, which shows some degree of similarity to the Nik system in several gram-negative bacteria (2,18,24,26), and (ii) a single-component carrier encoded by the ureH gene, displaying homology to polypeptides of the nickel-cobalt transporter family exemplified by HoxN (13 (22) and an ABC transporter (17). However, the latter has not been proven to be specific for nickel.…”

Section: Discussionmentioning

confidence: 99%

“…Expression of the E. coli nik operon is activated (in the absence of oxygen) by the global regulatory protein FNR and repressed (in the presence of high nickel concentrations) by the nickel-responsive regulator NikR, which is functionally similar to the Fur ferric ion uptake regulator (5,8,39). Similar ABC transport systems with significant homology to the E. coli Nik proteins have recently been described for two human pathogens, Vibrio parahaemolyticus (26) and Brucella suis (18).…”

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confidence: 92%

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Genes Encoding Specific Nickel Transport Systems Flank the Chromosomal Urease Locus of Pathogenic Yersiniae

2002

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The transition metal nickel is an essential cofactor for a number of bacterial enzymes, one of which is urease. Prior to its incorporation into metalloenzyme active sites, nickel must be imported into the cell. Here, we report identification of two loci corresponding to nickel-specific transport systems in the gram-negative, ureolytic bacterium Yersinia pseudotuberculosis. The loci are located on each side of the chromosomal urease gene cluster ureABCEFGD and have the same orientation as the latter. The yntABCDE locus upstream of the ure genes encodes five predicted products with sequence homology to ATP-binding cassette nickel permeases present in several gram-negative bacteria. The ureH gene, located downstream of ure, encodes a single-component carrier which displays homology to polypeptides of the nickel-cobalt transporter family. Transporters with homology to these two classes are also present (again in proximity to the urease locus) in the other two pathogenic yersiniae, Y. pestis and Y. enterocolitica. An Escherichia coli nikA insertion mutant recovered nickel uptake ability following heterologous complementation with either the ynt or the ureH plasmid-borne gene of Y. pseudotuberculosis, demonstrating that each carrier is necessary and sufficient for nickel transport. Deletion of ynt in Y. pseudotuberculosis almost completely abolished bacterial urease activity, whereas deletion of ureH had no effect. Nevertheless, rates of nickel transport were significantly altered in both ynt and ureH mutants. Furthermore, the ynt ureH double mutant was totally devoid of nickel uptake ability, thus indicating that Ynt and UreH constitute the only routes for nickel entry. Both Ynt and UreH show selectivity for Ni 2؉ ions. This is the first reported identification of genes coding for both kinds of nickel-specific permeases situated adjacent to the urease gene cluster in the genome of a microorganism.Urease, produced by a wide range of eukaryotic and prokaryotic organisms, is an enzyme that hydrolyzes urea to give ammonia and carbamate. This multimeric enzyme requires nickel for activity and is thus classed as a metalloenzyme (23). Bacteria have devised elaborate mechanisms for acquisition and incorporation of the divalent nickel ion. Nickel uptake constitutes the first step in this process. Diffusion of cations through the outer membrane of gram-negative bacteria occurs preferentially via the OmpC and OmpF porins (25). Translocation of nickel through the cytoplasmic membrane is then mediated by the nonspecific CorA and Mgt magnesium transport systems (33) and/or high-affinity, nickel-specific permeases (12). To date, two classes of high-affinity nickel transporters have been described for bacteria. The first, the Nik system, was originally identified as being essential for hydrogenase activity in Escherichia coli and is a member of the ATP-binding cassette (ABC) family. It consists of five components: a periplasmic binding protein (NikA) exhibiting high specificity for nickel, two integral cytoplasmic membrane proteins ...

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Identification of thenikGene Cluster ofBrucella suis: Regulation and Contribution to Urease Activity

Cited by 57 publications

References 44 publications

Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters

Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters

Conserved Low-Affinity Nickel-Binding Amino Acids Are Essential for the Function of the Nickel Permease NixA of Helicobacter pylori

Genes Encoding Specific Nickel Transport Systems Flank the Chromosomal Urease Locus of Pathogenic Yersiniae

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