Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans

Journal Article · · Journal of Biological Chemistry
 [1];  [2];  [2];  [2]
  1. New Mexico State Univ., Las Cruces, NM (United States); DOE Office of Scientific and Technical Information (OSTI)
  2. New Mexico State Univ., Las Cruces, NM (United States)
Here, ATP-binding cassette (ABC) transporters of the cluster 9 family are ubiquitous among bacteria and essential for acquiring Zn2+ and Mn2+ from the environment or, in the case of pathogens, from the host. These rely on a substrate-binding protein (SBP) to coordinate the relevant metal with high affinity and specificity and subsequently release it to a membrane permease for translocation into the cytoplasm. Although a number of cluster 9 SBP structures have been determined, the structural attributes conferring Zn2+ or Mn2+ specificity remain ambiguous. Here we describe the gene expression profile, in vitro metal binding properties, and crystal structure of a new cluster 9 SBP from Paracoccus denitrificans we have called AztC. Although all of our results strongly indicate Zn2+ over Mn2+ specificity, the Zn2+ ion is coordinated by a conserved Asp residue only observed to date as a metal ligand in Mn2+-specific SBPs. The unusual sequence properties of this protein are shared among close homologues, including members from the human pathogens Klebsiella pneumonia and Enterobacter aerogenes, and would seem to suggest a subclass of Zn2+-specific transporters among the cluster 9 family. In any case, the unusual coordination environment of AztC expands the already considerable range of those available to Zn2+-specific SBPs and highlights the presence of a His-rich loop as the most reliable indicator of Zn2+ specificity.
Research Organization:
Univ. of California, Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1347699
Journal Information:
Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 19 Vol. 290; ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (57)

Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase journal June 1996
Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli journal November 2007
Metal ions in biological catalysis: from enzyme databases to general principles journal July 2008
A new family of high-affinity ABC manganese and zinc permeases journal April 2001
The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae, encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins journal February 1997
The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein journal December 1998
A deliberate approach to screening for initial crystallization conditions of biological macromolecules journal April 2003
Structural Determinants of Metal Specificity in the Zinc Transport Protein ZnuA from Synechocystis 6803 journal November 2003
The MntC Crystal Structure Suggests that Import of Mn2+ in Cyanobacteria is Redox Controlled journal May 2005
Structural Analysis of ABC-family Periplasmic Zinc Binding Protein Provides New Insights Into Mechanism of Ligand Uptake and Release journal April 2007
Crystal Structure of the Zinc-binding Transport Protein ZnuA from Escherichia coli Reveals an Unexpected Variation in Metal Coordination journal May 2007
The X-ray Structure of the Zinc Transporter ZnuA from Salmonella enterica Discloses a Unique Triad of Zinc-Coordinating Histidines journal June 2011
Three-Dimensional Structure and Biophysical Characterization of Staphylococcus aureus Cell Surface Antigen–Manganese Transporter MntC journal September 2013
Use of the amicyanin signal sequence for efficient periplasmic expression in E. coli of a human antibody light chain variable domain journal April 2015
The Phenix software for automated determination of macromolecular structures journal September 2011
Spectroscopic Determination of Tryptophan and Tyrosine in Proteins * journal July 1967
MauG, a Novel Diheme Protein Required for Tryptophan Tryptophylquinone Biogenesis journal June 2003
Metal-Binding Characteristics of the Amino-Terminal Domain of ZntA:  Binding of Lead Is Different Compared to Cadmium and Zinc journal April 2005
Metal-Binding Affinity of the Transmembrane Site in ZntA:  Implications for Metal Selectivity journal January 2006
Conserved Aspartic Acid 714 in Transmembrane Segment 8 of the ZntA Subgroup of P 1B -Type ATPases Is a Metal-Binding Residue journal May 2006
Metal Binding Studies and EPR Spectroscopy of the Manganese Transport Regulator MntR journal December 2006
Possible Regulatory Role for the Histidine-Rich Loop in the Zinc Transport Protein, ZnuA , journal July 2007
Crystal Structure and Metal Binding Properties of the Lipoprotein MtsA, Responsible for Iron Transport in Streptococcus pyogenes journal July 2009
Imperfect coordination chemistry facilitates metal ion release in the Psa permease journal November 2013
SignalP 4.0: discriminating signal peptides from transmembrane regions journal September 2011
In-gel digestion for mass spectrometric characterization of proteins and proteomes journal December 2006
Bacterial ATP-driven transporters of transition metals: physiological roles, mechanisms of action, and roles in bacterial virulence journal January 2011
Apo, Zn2+-bound and Mn2+-bound structures reveal ligand-binding properties of SitA from the pathogen Staphylococcus pseudintermedius journal November 2014
The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague journal April 1999
Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens journal February 2013
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism journal November 2013
Metal Ion Binding and Coordination Geometry for Wild Type and Mutants of Metallo-β-lactamase from Bacillus cereus 569/H/9 (BcII) : A COMBINED THERMODYNAMIC, KINETIC, AND SPECTROSCOPIC APPROACH journal September 2001
Severe Zinc Depletion of Escherichia coli: ROLES FOR HIGH AFFINITY ZINC BINDING BY ZinT, ZINC TRANSPORT AND ZINC-INDEPENDENT PROTEINS journal April 2009
In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection journal May 2002
Phaser crystallographic software journal July 2007
Coot model-building tools for molecular graphics journal November 2004
Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination journal February 2008
Overview of the CCP 4 suite and current developments journal March 2011
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM journal March 2011
REFMAC 5 for the refinement of macromolecular crystal structures journal March 2011
Structural changes in a cryo-cooled protein crystal owing to radiation damage journal March 2000
Arginine 116 stabilizes the entrance to the metal ion-binding site of the MntC protein journal February 2013
The solute-binding component of a putative Mn(II) ABC transporter (MntA) is a novel Bacillus anthracis virulence determinant: Role of MntA in anthrax pathogenesis journal September 2005
The general transition metal (Tro) and Zn 2+ (Znu) transporters in Treponema pallidum : analysis of metal specificities and expression profiles journal July 2007
Calprotectin-Mediated Zinc Chelation as a Biostatic Mechanism in Host Defence journal November 1995
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis journal June 2001
MntABC and MntH Contribute to Systemic Staphylococcus aureus Infection by Competing with Calprotectin for Nutrient Manganese journal July 2013
High-Affinity Zn2+ Uptake System ZnuABC Is Required for Bacterial Zinc Homeostasis in Intracellular Environments and Contributes to the Virulence of Salmonella enterica journal October 2007
The Zinc-Responsive Regulator Zur Controls a Zinc Uptake System and Some Ribosomal Proteins in Streptomyces coelicolor A3(2) journal April 2007
TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence journal July 2011
The Crystal Structure of Zn(II)-Free Treponema pallidum TroA, a Periplasmic Metal-Binding Protein, Reveals a Closed Conformation journal April 2002
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. journal January 1993
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria journal June 1993
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria journal June 1993
Insight into the Interaction of Metal Ions with TroA from Streptococcus suis journal May 2011
A Molecular Mechanism for Bacterial Susceptibility to Zinc journal November 2011
Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence journal January 2013

Cited By (3)

Two ABC Transporters and a Periplasmic Metallochaperone Participate in Zinc Acquisition in Paracoccus denitrificans journal October 2018
Crystal structures of AztD provide mechanistic insights into direct zinc transfer between proteins journal August 2019
In silico Study of Iron, Zinc and Copper Binding Proteins of Pseudomonas syringae pv. lapsa: Emphasis on Secreted Metalloproteins journal August 2018

Similar Records

The NADH-binding subunit of the energy-transducing NADH-ubiquinone oxidoreductase of Paracoccus denitrificans: Gene cloning and deduced primary structure
Journal Article · Tue Jul 02 00:00:00 EDT 1991 · Biochemistry; (United States) · OSTI ID:5032398

Identification of the NADH-binding subunit of NADH-ubiquinone oxidoreductase of Paracoccus denitrificans
Journal Article · Tue Jun 12 00:00:00 EDT 1990 · Biochemistry; (United States) · OSTI ID:5393675

Structure and Function of the Zinc Binding Protein ZrgA from Vibrio cholerae
Journal Article · Wed Dec 28 19:00:00 EST 2022 · International Journal of Molecular Sciences (Online) · OSTI ID:2471006