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Structures of the Escherichia coli transcription activator and regulator of diauxie, XylR: an AraC DNA-binding family member with a LacI/GalR ligand-binding domain

Journal Article · · Nucleic Acids Research
DOI:https://doi.org/10.1093/nar/gks1207· OSTI ID:1625499
 [1];  [2];  [2];  [2]
  1. Univ. of Texas, Houston, TX (United States); DOE/OSTI
  2. Duke Univ., Durham, NC (United States)

Escherichia coli can rapidly switch to the metabolism of L-arabinose and D-xylose in the absence of its preferred carbon source, glucose, in a process called carbon catabolite repression. Transcription of the genes required for L-arabinose and D-xylose consumption is regulated by the sugar-responsive transcription factors, AraC and XylR. E. coli represents a promising candidate for biofuel production through the metabolism of hemicellulose, which is composed of D-xylose and L-arabinose. Understanding the L-arabinose/D-xylose regulatory network is key for such biocatalyst development. Unlike AraC, which is a well-studied protein, little is known about XylR. To gain insight into XylR function, we performed biochemical and structural studies. XylR contains a C-terminal AraC-like domain. However, its N-terminal D-xylose-binding domain contains a periplasmic-binding protein (PBP) fold with structural homology to LacI/GalR transcription regulators. Like LacI/GalR proteins, the XylR PBP domain mediates dimerization. However, unlike LacI/GalR proteins, which dimerize in a parallel, side-to-side manner, XylR PBP dimers are antiparallel. Strikingly, D-xylose binding to this domain results in a helix to strand transition at the dimer interface that reorients both DNA-binding domains, allowing them to bind and loop distant operator sites. Thus, the combined data reveal the ligand-induced activation mechanism of a new family of DNA-binding proteins.

Research Organization:
Duke University, Durham, NC (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1625499
Journal Information:
Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 3 Vol. 41; ISSN 0305-1048
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (51)

AraC protein: A love-hate relationship journal February 2003
Solution structure of the DNA binding domain of AraC protein journal October 2009
Mica Functionalization for Imaging of DNA and Protein-DNA Complexes with Atomic Force Microscopy book January 2012
Mechanism of corepressor-mediated specific DNA binding by the purine repressor journal October 1995
Structural Basis for Allosteric Control of the Transcription Regulator CcpA by the Phosphoprotein HPr-Ser46-P journal September 2004
Regulation of the L-arabinose operon of Escherichia coli journal December 2000
Silatrane-based surface chemistry for immobilization of DNA, protein-DNA complexes and other biological materials journal October 2003
In situ AFM Study of Amelogenin Assembly and Disassembly Dynamics on Charged Surfaces Provides Insights on Matrix Protein Self-Assembly journal November 2011
Mechanism responsible for glucose-lactose diauxie in Escherichia coli : challenge to the cAMP model journal March 1996
Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes journal February 2010
A novel DNA-binding motif in MarA: The first structure for an AraC family transcriptional activator journal September 1998
Atomic force microscopic demonstration of DNA looping by GalR and HU journal February 1997
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use journal November 2004
Features and development of Coot journal March 2010
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination journal September 1998
Automated MAD and MIR structure solution journal April 1999
Integration of macromolecular diffraction data journal October 1999
Utilization of d-ribose through d-xylose transporter journal June 1998
Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization journal April 2002
AraC protein, regulation of the l-arabinose operon in Escherichia coli , and the light switch mechanism of AraC action journal September 2010
The Whole Lactose Repressor journal March 1996
Structural Basis for Ligand-Regulated Oligomerization of AraC journal April 1997
Crystal structure of LacI member, PurR, bound to DNA: minor groove binding by alpha helices journal November 1994
Supplementation of Intracellular XylR Leads to Coutilization of Hemicellulose Sugars journal January 2012
Regulation of d-Xylose Metabolism in Caulobacter crescentus by a LacI-Type Repressor journal October 2007
Organization and regulation of the D-xylose operons in Escherichia coli K-12: XylR acts as a transcriptional activator. journal January 1997
Arac/XylS family of transcriptional regulators journal December 1997
The venus flytrap of periplasmic binding proteins: An ancient protein module present in multiple drug receptors journal June 1999
Fluorescence polarization analysis of protein-DNA and protein-protein interactions. journal June 1996
Simultaneous consumption of pentose and hexose sugars: an optimal microbial phenotype for efficient fermentation of lignocellulosic biomass journal September 2010
Bacterial Periplasmic Binding Protein Tertiary Structures journal September 1989
Regulation of the L-arabinose operon of Escherichia coli journal December 2000
Silatrane-based surface chemistry for immobilization of DNA, protein-DNA complexes and other biological materials journal October 2003
Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization journal April 2002
Crystal structure of the Escherichia coli Rob transcription factor in complex with DNA journal May 2000
Charting a course through RNA polymerase journal September 2000
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome journal December 2019
Conformational exchange in the potassium channel blocker ShK journal December 2019
Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins journal December 2008
Integration of macromolecular diffraction data book October 2006
Integration of macromolecular diffraction data book April 2012
Features and development of Coot journal March 2010
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination journal September 1998
Automated MAD and MIR structure solution journal April 1999
Integration of macromolecular diffraction data journal October 1999
DNA looping and unlooping by AraC protein journal October 1990
Crystal Structure of the Lactose Operon Repressor and Its Complexes with DNA and Inducer journal March 1996
Arac/XylS family of transcriptional regulators. journal January 1997
Regulation of Arabinose and Xylose Metabolism in Escherichia coli journal December 2009
Supplementation of Intracellular XylR Leads to Coutilization of Hemicellulose Sugars journal January 2012
Regulation of d-Xylose Metabolism in Caulobacter crescentus by a LacI-Type Repressor journal October 2007

Cited By (8)

AutA and AutR, Two Novel Global Transcriptional Regulators, Facilitate Avian Pathogenic Escherichia coli Infection journal April 2016
A large family of anti‐activators accompanying XylS/AraC family regulatory proteins journal May 2016
Functional Mechanism of the Efflux Pumps Transcription Regulators From Pseudomonas aeruginosa Based on 3D Structures journal June 2018
Metabolic engineering strategies for improving xylitol production from hemicellulosic sugars journal July 2013
HipBA–promoter structures reveal the basis of heritable multidrug tolerance journal July 2015
Experimental evolution reveals an effective avenue to release catabolite repression via mutations in XylR journal June 2017
Molecular mechanisms of xylose utilization by P seudomonas fluorescens : overlapping genetic responses to xylose, xylulose, ribose and mannitol: Xylose utilization in Pseudomonas journal August 2015
Functional Characterization of the Mannitol Promoter of Pseudomonas fluorescens DSM 50106 and Its Application for a Mannitol-Inducible Expression System for Pseudomonas putida KT2440 journal July 2015

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