Article

Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: Evidence for a novel group of ATP-binding cassette transporters

The Burnham Institute, 10901 N. Torrey Pines Road, La Jolla, CA 92037, USA.
Journal of Bacteriology (Impact Factor: 2.69). 02/2006; 188(1):317-27. DOI: 10.1128/JB.188.1.317-327.2006
Source: PubMed

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.

Download full-text

Full-text

Available from: Peter Hebbeln, Oct 10, 2014
0 Followers
 · 
97 Views
 · 
15 Downloads
  • Source
    • "Indeed, several organisms, such as bacteria, algae, yeast, and fungi are capable of reducing metal ions through metalloregulatory mechanism upon exposure to metal ions (Dameron et al. 1989; Labrenz et al. 2000; Mukherjee et al. 2001b; Kang et al. 2008). Details on the cellular mechanisms for the uptake and storage of metal ions by specific transporters and their related enzymes have been described previously (Vignais et al. 2001; Clugston et al. 2004; Kuchar and Hausinger 2004; Rodionov et al. 2006). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Metal nanoparticles are garnering considerable attention owing to their high potential for use in various applications in the material, electronics, and energy industries. Recent research efforts have focused on the biosynthesis of metal nanomaterials using microorganisms rather than traditional chemical synthesis methods. Microorganisms have evolved to possess molecular machineries for detoxifying heavy metals, mainly by employing metal-binding proteins and peptides. Biosynthesis of diverse metal nanoparticles has recently been demonstrated using such heavy metal detoxification systems in microorganisms, which provides several advantages over the traditional chemical synthesis methods. First, metal nanoparticles can be synthesized at mild temperatures, such as at room temperature, with less energy input. Second, no toxic chemicals or reagents are needed, and thus the process is environmentally friendly. Third, diverse metal nanoparticles, including those that have never been chemically synthesized, can be biosynthesized. Here, we review the strategies for the biosynthesis of metal nanoparticles using microorganisms, and provide future prospects.
    Applied Microbiology and Biotechnology 08/2015; DOI:10.1007/s00253-015-6904-7 · 3.81 Impact Factor
  • Source
    • "It has been extensively documented that some species of bacteria contain dedicated transporters that favor the uptake of Ni(II) and Co(II). These transporters include the nikABCDE system found in E. coli[13], the NiCoT family found in eubacteria, archaea and fungi [14] and some ABC transporters [15,16]. Using genetic techniques, it has been proven that such transporters, which differ in their specificity towards Co(II) and Ni(II) [15,17,18], can be expressed in various bacterial species [17,19]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background Metal contamination is widespread and results from natural geogenic and constantly increasing anthropogenic sources (mainly mining and extraction activities, electroplating, battery and steel manufacturing or metal finishing). Consequently, there is a growing need for methods to detoxify polluted ecosystems. Industrial wastewater, surface water and ground water need to be decontaminated to alleviate the contamination of soils and sediments and, ultimately, the human food chain. In nuclear power plants, radioactive metals are produced; these metals need to be removed from effluents before they are released into the environment, not only for pollution prevention but also for waste minimization. Many physicochemical methods have been developed for metal removal from aqueous solutions, including chemical coagulation, adsorption, extraction, ion exchange and membrane separation; however, these methods are generally not metal selective. Bacteria, because they contain metal transporters, provide a potentially competitive alternative to the current use of expensive and high-volume ion-exchange resins. Results The feasibility of using bacterial biofilters as efficient tools for nickel and cobalt ions specific remediation was investigated. Among the factors susceptible to genetic modification in Escherichia coli, specific efflux and sequestration systems were engineered to improve its metal sequestration abilities. Genomic suppression of the RcnA nickel (Ni) and cobalt (Co) efflux system was combined with the plasmid-controlled expression of a genetically improved version of a specific metallic transporter, NiCoT, which originates from Novosphingobium aromaticivorans. The resulting strain exhibited enhanced nickel (II) and cobalt (II) uptake, with a maximum metal ion accumulation of 6 mg/g bacterial dry weight during 10 min of treatment. A synthetic adherence operon was successfully introduced into the plasmid carrying the improved NiCoT transporter, conferring the ability to form thick biofilm structures, especially when exposed to nickel and cobalt metallic compounds. Conclusions This study demonstrates the efficient use of genetic engineering to increase metal sequestration and biofilm formation by E. coli. This method allows Co and Ni contaminants to be sequestered while spatially confining the bacteria to an abiotic support. Biofiltration of nickel (II) and cobalt (II) by immobilized cells is therefore a promising option for treating these contaminants at an industrial scale.
    Journal of Biological Engineering 08/2014; 8:19. DOI:10.1186/1754-1611-8-19
  • Source
    • "All synthetic DNAs were verified by nucleotide sequencing. Mutant plasmids were introduced into E. coli XL1-Blue and nickel-uptake activity was determined as described6. Briefly, cells were grown in lysogeny broth (LB) over night, diluted 1:100 in LB supplemented with ampicillin (100 μg/ml), IPTG (1 mM) and 63NiCl2 (500 nM), and incubated under shaking at 37 °C for seven hours. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The energy-coupling factor (ECF) transporters are multi-subunit protein complexes that mediate uptake of transition-metal ions and vitamins in about 50% of the prokaryotes, including bacteria and archaea. Biological and structural studies have been focused on ECF transporters for vitamins, but the molecular mechanism by which ECF systems transport metal ions from the environment remains unknown. Here we report the first crystal structure of a NikM, TtNikM2, the substrate-binding component (S component) of an ECF-type nickel transporter from Thermoanaerobacter tengcongensis. In contrast to the structures of the vitamin-specific S proteins with six transmembrane segments (TSs), TtNikM2 possesses an additional TS at its N-terminal region, resulting in an extracellular N-terminus. The highly conserved N-terminal loop inserts into the center of TtNikM2 and occludes a region corresponding to the substrate-binding sites of the vitamin-specific S components. Nickel binds to NikM via its coordination to four nitrogen atoms, which are derived from Met1, His2 and His67 residues. These nitrogen atoms form an approximately square-planar geometry, similar to that of the metal ion-binding sites in the amino-terminal Cu(2+)- and Ni(2+)-binding (ATCUN) motif. Replacements of residues in NikM contributing to nickel coordination compromised the Ni-transport activity. Furthermore, systematic quantum chemical investigation indicated that this geometry enables NikM to also selectively recognize Co(2+). Indeed, the structure of TtNikM2 containing a bound Co(2+) ion has almost no conformational change compared to the structure that contains a nickel ion. Together, our data reveal an evolutionarily conserved mechanism underlying the metal selectivity of EcfS proteins, and provide insights into the ion-translocation process mediated by ECF transporters.Cell Research advance online publication 24 December 2013; doi:10.1038/cr.2013.172.
    Cell Research 12/2013; 24(3). DOI:10.1038/cr.2013.172 · 11.98 Impact Factor
Show more