title: Promiscuous nickel import in human pathogens: structure, thermodynamics, and evolution of extracytoplasmic nickel-binding proteins.
abstract: In human pathogenic bacteria, nickel is required for the activation of two enzymes, urease and [NiFe]-hydrogenase, necessary for host infection. Acquisition of Ni(II) is mediated by either permeases or ABC-importers, the latter including a subclass that involves an extracytoplasmic nickel-binding protein, Ni-BP. This study reports on the structure of three Ni-BPs from a diversity of human pathogens and on the existence of three new nickel-binding motifs. These are different from that previously described for Escherichia coli Ni-BP NikA, known to bind nickel via a nickelophore, and indicate a variegated ligand selectivity for Ni-BPs. The structures are consistent with ligand affinities measured in solution by calorimetry and challenge the hypothesis of a general requirement of nickelophores for nickel uptake by canonical ABC importers. Phylogenetic analyses showed that Ni-BPs have different evolutionary origins and emerged independently from peptide-binding proteins, possibly explaining the promiscuous behavior of this class of Ni(II) carriers.
authors.affiliation: University Grenoble Alpes, Institut de Biologie Structurale (IBS), 38044 Grenoble, France; CNRS, IBS, 38044 Grenoble, France; CEA, IBS, 38044 Grenoble, France.
authors.forename: Hugo
authors.initials: H
authors.lastname: Lebrette
authors.affiliation: Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, 43 Boulevard du 11 Novembre 1918, 69622 Villeurbanne, France.
authors.forename: Céline
authors.initials: C
authors.lastname: Brochier-Armanet
authors.affiliation: Laboratory of Bioinorganic Chemistry, Department of Pharmacy and Biotechnology, University of Bologna, Viale Giuseppe Fanin, 40, 40127 Bologna, Italy.
authors.forename: Barbara
authors.initials: B
authors.lastname: Zambelli
authors.affiliation: Département de Microbiologie, Unité Pathogenèse de Helicobacter, Institut Pasteur, 75724 Paris Cedex 15, France.
authors.forename: Hilde
authors.initials: H
authors.lastname: de Reuse
authors.affiliation: INRA, UMR 1319 Micalis, 78350 Jouy en Josas, France; Agro ParisTech, UMR Micalis, 78350 Jouy en Josas, France.
authors.forename: Elise
authors.initials: E
authors.lastname: Borezée-Durant
authors.affiliation: Laboratory of Bioinorganic Chemistry, Department of Pharmacy and Biotechnology, University of Bologna, Viale Giuseppe Fanin, 40, 40127 Bologna, Italy. Electronic address: stefano.ciurli@unibo.it.
authors.forename: Stefano
authors.initials: S
authors.lastname: Ciurli
authors.affiliation: University Grenoble Alpes, LCBM, 17, Avenue des Martyrs, 38054 Grenoble Cedex 09, France. Electronic address: christine.cavazza@cea.fr.
authors.forename: Christine
authors.initials: C
authors.lastname: Cavazza
mesh_terms: D020816:Amino Acid Motifs; D000595:Amino Acid Sequence; D001426:Bacterial Proteins / Q000737:chemistry* / Q000378:metabolism; D001665:Binding Sites; D001692:Biological Transport; D041021:Brucella suis / Q000737:chemistry / Q000472:pathogenicity; D016123:Campylobacter jejuni / Q000737:chemistry / Q000472:pathogenicity; D002352:Carrier Proteins / Q000737:chemistry* / Q000378:metabolism*; D018360:Crystallography, X-Ray; D019143:Evolution, Molecular; D008958:Models, Molecular; D008969:Molecular Sequence Data; D009532:Nickel / Q000378:metabolism*; D010802:Phylogeny; D011487:Protein Conformation; D013816:Thermodynamics; D015010:Yersinia pestis / Q000737:chemistry / Q000472:pathogenicity
chemical_list: D001426:Bacterial Proteins; D002352:Carrier Proteins; D009532:Nickel