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

Atypical chemoreceptor arrays accommodate high membrane curvature

Journal Article · · Nature Communications
The prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology. In all previously described species, chemoreceptors organize into a hexagonal (P6 symmetry) extended array. Here, we report an alternative symmetry (P2) of the chemotaxis apparatus that emerges from a strict linear organization of the histidine kinase CheA in Treponema denticola cells, which possesses arrays with the highest native curvature investigated thus far. Using cryo-ET, we reveal that Td chemoreceptor arrays assume an unusual arrangement of the supra-molecular protein assembly that has likely evolved to accommodate the high membrane curvature. The arrays have several atypical features, such as an extended dimerization domain of CheA and a variant CheW-CheR-like fusion protein that is critical for maintaining an ordered chemosensory apparatus. Furthermore, the previously characterized Td oxygen sensor ODP influences CheA ordering. These results suggest a greater diversity of the chemotaxis signaling system than previously thought.
Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Organization:
USDOE Office of Science (SC); National Institutes of Health (NIH); Dutch Research Council (NWO); European Union; National Institute of General Medical Sciences (NIGMS)
OSTI ID:
1767227
Alternate ID(s):
OSTI ID: 1770424
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 11; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
ENGLISH

References (47)

Dual-Axis Tomography: An Approach with Alignment Methods That Preserve Resolution journal December 1997
Structure of CheA, a Signal-Transducing Histidine Kinase journal January 1999
Molecular characterization of a chemotaxis operon in the oral spirochete, Treponema denticola journal May 1999
Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine journal April 1997
Angiotensin II induced CSF1 transcription is mediated by a crosstalk between different epigenetic factors in vascular endothelial cells journal January 2019
Crystal structure of scaffolding protein CheW from thermoanaerobacter tengcongensis journal October 2007
Cellular Architecture of Treponema pallidum: Novel Flagellum, Periplasmic Cone, and Cell Envelope as Revealed by Cryo Electron Tomography journal November 2010
Conformational Transitions that Enable Histidine Kinase Autophosphorylation and Receptor Array Integration journal December 2015
CTF determination and correction for low dose tomographic tilt series journal December 2009
Dynamo: A flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments journal May 2012
Dynamo Catalogue: Geometrical tools and data management for particle picking in subtomogram averaging of cryo-electron tomograms journal February 2017
A simplified erythromycin resistance cassette for Treponema denticola mutagenesis journal October 2010
Bacterial chemoreceptors: high-performance signaling in networked arrays journal January 2008
Structure of the Ternary Complex Formed by a Chemotaxis Receptor Signaling Domain, the CheA Histidine Kinase, and the Coupling Protein CheW As Determined by Pulsed Dipolar ESR Spectroscopy journal May 2010
The 3.2 Å Resolution Structure of a Receptor:CheA:CheW Signaling Complex Defines Overlapping Binding Sites and Key Residue Interactions within Bacterial Chemosensory Arrays journal May 2013
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life journal August 2018
Chemotaxis receptor recognition by protein methyltransferase CheR journal June 1998
Complete structure of the chemosensory array core signalling unit in an E. coli minicell strain journal February 2020
Structure and dynamics of the E. coli chemotaxis core signaling complex by cryo-electron tomography and molecular simulations journal January 2020
Universal architecture of bacterial chemoreceptor arrays journal September 2009
Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins journal February 2012
The source of high signal cooperativity in bacterial chemosensory arrays journal March 2016
Baseplate variability of Vibrio cholerae chemoreceptor arrays journal December 2018
A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species journal July 2019
High Specificity in CheR Methyltransferase Function: CheR2 OF PSEUDOMONAS PUTIDA IS ESSENTIAL FOR CHEMOTAXIS, WHEREAS CheR1 IS INVOLVED IN BIOFILM FORMATION journal May 2013
Clustering of highly homologous sequences to reduce the size of large protein databases journal March 2001
Jalview Version 2--a multiple sequence alignment editor and analysis workbench journal January 2009
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
SWISS-MODEL: an automated protein homology-modeling server journal July 2003
MiST 3.0: an updated microbial signal transduction database with an emphasis on chemosensory systems journal November 2019
WebLogo: A Sequence Logo Generator journal May 2004
XDS journal January 2010
Features and development of Coot journal March 2010
AMPLE : a cluster-and-truncate approach to solve the crystal structures of small proteins using rapidly computed ab initio models journal November 2012
Exploring the speed and performance of molecular replacement with AMPLE using QUARK ab initio protein models journal January 2015
Routine phasing of coiled-coil protein crystal structures with AMPLE journal February 2015
Two CheW coupling proteins are essential in a chemosensory pathway of Borrelia burgdorferi: Borrelia burgdorferi chemotaxis journal July 2012
The mobility of two kinase domains in the E scherichia coli chemoreceptor array varies with signalling state journal July 2013
pyrF as a Counterselectable Marker for Unmarked Genetic Manipulations in Treponema denticola journal December 2015
Borrelia burgdorferi Needs Chemotaxis To Establish Infection in Mammals and To Accomplish Its Enzootic Cycle journal April 2012
Purification and characterization of an enzyme produced by Treponema denticola capable of hydrolyzing synthetic trypsin substrates. journal January 1986
Chemoreceptors and Flagellar Motors Are Subterminally Located in Close Proximity at the Two Cell Poles in Spirochetes journal March 2011
Three-Dimensional Structures of Pathogenic and Saprophytic Leptospira Species Revealed by Cryo-Electron Tomography journal January 2012
Short FtsZ filaments can drive asymmetric cell envelope constriction at the onset of bacterial cytokinesis journal April 2017
‘One is the loneliest number’; are we witnessing the death throes of the single-author research paper in the field of biological invasions? journal January 2019
Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling journal March 2014
CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling journal November 2015

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

A di-iron protein recruited as an Fe[II] and oxygen sensor for bacterial chemotaxis functions by stabilizing an iron-peroxy species
Journal Article · Wed Jul 03 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1564316