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

A direct-sensing galactose chemoreceptor recently evolved in invasive strains of Campylobacter jejuni

Journal Article · · Nature Communications
DOI:https://doi.org/10.1038/ncomms13206· OSTI ID:1330560
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [1]
  1. Griffith Univ., Queensland (Australia)
  2. Univ. of Tennessee, Knoxville, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

A rare chemotaxis receptor, Tlp11, has been previously identified in invasive strains of Campylobacter jejuni, the most prevalent cause of bacterial gastroenteritis worldwide. Here we use glycan and small-molecule arrays, as well as surface plasmon resonance, to show that Tlp11 specifically interacts with galactose. Tlp11 is required for the chemotactic response of C. jejuni to galactose, as shown using wild type, allelic inactivation and addition mutants. The inactivated mutant displays reduced virulence in vivo, in a model of chicken colonization. The Tlp11 sensory domain represents the first known sugar-binding dCache_1 domain, which is the most abundant family of extracellular sensors in bacteria. The Tlp11 signalling domain interacts with the chemotaxis scaffolding proteins CheV and CheW, and comparative genomic analysis indicates a likely recent evolutionary origin for Tlp11. Lastly, we propose to rename Tlp11 as CcrG, Campylobacter ChemoReceptor for Galactose.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1330560
Journal Information:
Nature Communications, Journal Name: Nature Communications Vol. 7; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (62)

The use of transepithelial models to examine host–pathogen interactions journal February 2003
CheY‐mediated modulation of Campylobacter jejuni virulence journal March 1997
Ancient chemoreceptors retain their flexibility journal February 2007
The Bacillus subtilis Chemoreceptor McpC Senses Multiple Ligands Using Two Discrete Mechanisms journal October 2012
Experimental Campylobacter jejuni Infection in Humans journal March 1988
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
The HHpred interactive server for protein homology detection and structure prediction journal July 2005
The MiST2 database: a comprehensive genomics resource on microbial signal transduction journal November 2009
The Pfam protein families database journal November 2011
CDD: conserved domains and protein three-dimensional structure journal November 2012
Pathogenesis of Enteric Infection by Campylobacter journal January 1997
Campylobacter jejuni proteins Cj0952c and Cj0951c affect chemotactic behaviour towards formic acid and are important for invasion of host cells journal October 2010
Comparison of 2-day-old and 14-day-old chicken colonization models for Campylobacter jejuni journal February 2007
Origins and Diversification of a Complex Signal Transduction System in Prokaryotes journal June 2010
Sinorhizobium meliloti Chemoreceptor McpU Mediates Chemotaxis toward Host Plant Exudates through Direct Proline Sensing journal March 2014
Mlp24 (McpX) of Vibrio cholerae Implicated in Pathogenicity Functions as a Chemoreceptor for Multiple Amino Acids journal July 2012
Chemotactic behavior of Campylobacter jejuni. journal January 1988
Cell association and invasion of Caco-2 cells by Campylobacter jejuni. journal January 1994
Phenotypic and Genotypic Evidence for L-Fucose Utilization by Campylobacter jejuni journal December 2010
Identification of Campylobacter jejuni Promoter Sequences journal February 1998
MUC1 cell surface mucin is a critical element of the mucosal barrier to infection journal August 2007
Cache Domains That are Homologous to, but Different from PAS Domains Comprise the Largest Superfamily of Extracellular Sensors in Prokaryotes journal April 2016
Differential Carbohydrate Recognition by Campylobacter jejuni Strain 11168: Influences of Temperature and Growth Conditions journal March 2009
Characterisation of a Multi-ligand Binding Chemoreceptor CcmL (Tlp3) of Campylobacter jejuni journal January 2014
Campylobacter jejuni— An Emerging Foodborne Pathogen journal February 1999
Insight into the sporulation phosphorelay: Crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD : The Crystal Structure of the KinD Sensor Domain journal March 2013
Identification of Proteins Required for the Internalization of Campylobacter Jejuni into Cultured Mammalian Cells book January 1999
A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. journal February 1988
The use of transepithelial models to examine host–pathogen interactions journal February 2003
Bacterial chemoreceptors: high-performance signaling in networked arrays journal January 2008
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins journal March 2021
Current epidemiological issues in human campylobacteriosis journal June 2001
Identification and molecular cloning of a gene encoding a fibronectin‐binding protein (CadF) from Campylobacter jejuni journal June 1997
A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176: C. jejuni capsular phase variation journal May 2001
Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors journal February 2007
L-Fucose utilization provides Campylobacter jejuni with a competitive advantage journal April 2011
Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. journal January 1979
A PAS Domain Binds Asparagine in the Chemotaxis Receptor McpB in Bacillus subtilis journal October 2009
The Bacillus subtilis Chemoreceptor McpC Senses Multiple Ligands Using Two Discrete Mechanisms journal October 2012
A PAS Domain Binds Asparagine in the Chemotaxis Receptor McpB in Bacillus subtilis journal October 2009
Epidemiologic and Clinical Features of Campylobacter jejuni Infections journal December 1997
Early Colonic Damage and Invasion of Campylobacter jejuni in Experimentally Challenged Infant Macaca mulatta journal July 1993
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 journal October 2013
Identification of hyperinvasive Campylobacter jejuni strains isolated from poultry and human clinical sources journal May 2008
JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells: Novel adhesin of C. jejuni journal March 2001
Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni: The aspartate receptor of Campylobacter jejuni journal December 2009
Comparison of 2-day-old and 14-day-old chicken colonization models for Campylobacter jejuni journal February 2007
Paralogous chemoreceptors mediate chemotaxis towards protein amino acids and the non-protein amino acid gamma-aminobutyrate (GABA): Amino acid chemoreceptors of journal May 2013
Sinorhizobium meliloti Chemoreceptor McpU Mediates Chemotaxis toward Host Plant Exudates through Direct Proline Sensing journal March 2014
Mlp24 (McpX) of Vibrio cholerae Implicated in Pathogenicity Functions as a Chemoreceptor for Multiple Amino Acids journal July 2012
Chemotactic behavior of Campylobacter jejuni. journal January 1988
Cell association and invasion of Caco-2 cells by Campylobacter jejuni. journal January 1994
Campylobacter jejuni motility and invasion of Caco-2 cells. journal January 1995
Involvement of a Plasmid in Virulence of Campylobacter jejuni 81-176 journal August 2000
Phenotypic and Genotypic Evidence for L-Fucose Utilization by Campylobacter jejuni journal December 2010
Identification of Campylobacter jejuni Promoter Sequences journal February 1998
Campylobacter jejuni motility and invasion of Caco-2 cells. journal January 1995
Involvement of a Plasmid in Virulence of Campylobacter jejuni 81-176 journal August 2000
MUC1 cell surface mucin is a critical element of the mucosal barrier to infection journal August 2007
Variation of chemosensory receptor content of Campylobacter jejuni strains and modulation of receptor gene expression under different in vivo and in vitro growth conditions journal January 2012
Campylobacter infection of commercial poultry: -EN- -FR- -ES- journal August 2000

Cited By (13)

Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut journal July 2018
Diversity of transducer-like proteins (Tlps) in Campylobacter journal March 2019
Parallel quorum-sensing system in Vibrio cholerae prevents signal interference inside the host journal February 2020
Phylogenetic and Protein Sequence Analysis of Bacterial Chemoreceptors book January 2018
Induced root-secreted d-galactose functions as a chemoattractant and enhances the biofilm formation of Bacillus velezensis SQR9 in an McpA-dependent manner journal December 2019
Glycointeractions in bacterial pathogenesis journal April 2018
Campylobacter jejuni: collective components promoting a successful enteric lifestyle journal June 2018
A peculiar case of Campylobacter jejuni attenuated aspartate chemosensory mutant, able to cause pathology and inflammation in avian and murine model animals journal August 2018
The effect of bacterial chemotaxis on host infection and pathogenicity journal October 2017
Role of the Campylobacter jejuni cheVAWY chemotaxis genes in chemotactic motility and biofilm formation journal November 2020
Assigning a role for chemosensory signal transduction in Campylobacter jejuni biofilms using a combined omics approach journal December 2019
The novel regulators CheP and CheQ control the core chemotaxis operon cheVAW in Campylobacter jejuni journal November 2018
Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction journal May 2017

Similar Records

Evolutionary genomics suggests that CheV is an additional adaptor for accommodating specific chemoreceptors within the chemotaxis signaling complex
Journal Article · Wed Feb 03 23:00:00 EST 2016 · PLoS Computational Biology (Online) · OSTI ID:1327747