Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes

Gliding motility using cell surface adhesins, and export of proteins by the type IX secretion system (T9SS) are two phylum-specific features of the Bacteroidetes. Both of these processes are energized by the GldLM motor complex, which transduces the proton motive force at the inner membrane into mec...

Full description

Bibliographic Details
Main Authors: Hennell James, R, Deme, JC, Hunter, A, Berks, BC, Lea, SM
Format: Journal article
Language:English
Published: American Society for Microbiology 2022
_version_ 1826308435794198528
author Hennell James, R
Deme, JC
Hunter, A
Berks, BC
Lea, SM
author_facet Hennell James, R
Deme, JC
Hunter, A
Berks, BC
Lea, SM
author_sort Hennell James, R
collection OXFORD
description Gliding motility using cell surface adhesins, and export of proteins by the type IX secretion system (T9SS) are two phylum-specific features of the Bacteroidetes. Both of these processes are energized by the GldLM motor complex, which transduces the proton motive force at the inner membrane into mechanical work at the outer membrane. We previously used cryo-electron microscopy to solve the structure of the GldLM motor core from Flavobacterium johnsoniae at 3.9-Å resolution (R. Hennell James, J. C. Deme, A. Kjaer, F. Alcock, et al., Nat Microbiol 6:221–233, 2021, https://dx.doi.org/10.1038/s41564-020-00823-6). Here, we present structures of homologous complexes from a range of pathogenic and environmental Bacteroidetes species at up to 3.0-Å resolution. These structures show that the architecture of the GldLM motor core is conserved across the Bacteroidetes phylum, although there are species-specific differences at the N terminus of GldL. The resolution improvements reveal a cage-like structure that ties together the membrane-proximal cytoplasmic region of GldL and influences gliding function. These findings add detail to our structural understanding of bacterial ion-driven motors that drive the T9SS and gliding motility.<br> IMPORTANCE Many bacteria in the Bacteroidetes phylum use the type IX secretion system to secrete proteins across their outer membrane. Most of these bacteria can also glide across surfaces using adhesin proteins that are propelled across the cell surface. Both secretion and gliding motility are driven by the GldLM protein complex, which forms a nanoscale electrochemical motor. We used cryo-electron microscopy to study the structure of the GldLM protein complex from different species, including the human pathogens Porphyromonas gingivalis and Capnocytophaga canimorsus. The organization of the motor is conserved across species, but we find species-specific structural differences and resolve motor features at higher resolution. This work improves our understanding of the type IX secretion system, which is a virulence determinant in human and animal diseases.
first_indexed 2024-03-07T07:19:28Z
format Journal article
id oxford-uuid:33f904e2-4cb3-404e-a6a4-a3f636fc6e27
institution University of Oxford
language English
last_indexed 2024-03-07T07:19:28Z
publishDate 2022
publisher American Society for Microbiology
record_format dspace
spelling oxford-uuid:33f904e2-4cb3-404e-a6a4-a3f636fc6e272022-09-21T10:32:53ZStructures of the Type IX Secretion/gliding motility motor from across the phylum BacteroidetesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:33f904e2-4cb3-404e-a6a4-a3f636fc6e27EnglishSymplectic ElementsAmerican Society for Microbiology2022Hennell James, RDeme, JCHunter, ABerks, BCLea, SMGliding motility using cell surface adhesins, and export of proteins by the type IX secretion system (T9SS) are two phylum-specific features of the Bacteroidetes. Both of these processes are energized by the GldLM motor complex, which transduces the proton motive force at the inner membrane into mechanical work at the outer membrane. We previously used cryo-electron microscopy to solve the structure of the GldLM motor core from Flavobacterium johnsoniae at 3.9-Å resolution (R. Hennell James, J. C. Deme, A. Kjaer, F. Alcock, et al., Nat Microbiol 6:221–233, 2021, https://dx.doi.org/10.1038/s41564-020-00823-6). Here, we present structures of homologous complexes from a range of pathogenic and environmental Bacteroidetes species at up to 3.0-Å resolution. These structures show that the architecture of the GldLM motor core is conserved across the Bacteroidetes phylum, although there are species-specific differences at the N terminus of GldL. The resolution improvements reveal a cage-like structure that ties together the membrane-proximal cytoplasmic region of GldL and influences gliding function. These findings add detail to our structural understanding of bacterial ion-driven motors that drive the T9SS and gliding motility.<br> IMPORTANCE Many bacteria in the Bacteroidetes phylum use the type IX secretion system to secrete proteins across their outer membrane. Most of these bacteria can also glide across surfaces using adhesin proteins that are propelled across the cell surface. Both secretion and gliding motility are driven by the GldLM protein complex, which forms a nanoscale electrochemical motor. We used cryo-electron microscopy to study the structure of the GldLM protein complex from different species, including the human pathogens Porphyromonas gingivalis and Capnocytophaga canimorsus. The organization of the motor is conserved across species, but we find species-specific structural differences and resolve motor features at higher resolution. This work improves our understanding of the type IX secretion system, which is a virulence determinant in human and animal diseases.
spellingShingle Hennell James, R
Deme, JC
Hunter, A
Berks, BC
Lea, SM
Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title_full Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title_fullStr Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title_full_unstemmed Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title_short Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes
title_sort structures of the type ix secretion gliding motility motor from across the phylum bacteroidetes
work_keys_str_mv AT hennelljamesr structuresofthetypeixsecretionglidingmotilitymotorfromacrossthephylumbacteroidetes
AT demejc structuresofthetypeixsecretionglidingmotilitymotorfromacrossthephylumbacteroidetes
AT huntera structuresofthetypeixsecretionglidingmotilitymotorfromacrossthephylumbacteroidetes
AT berksbc structuresofthetypeixsecretionglidingmotilitymotorfromacrossthephylumbacteroidetes
AT leasm structuresofthetypeixsecretionglidingmotilitymotorfromacrossthephylumbacteroidetes