Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics

ABSTRACT The type II secretion system (T2SS) releases large folded exoproteins across the envelope of many Gram-negative pathogens. This secretion process therefore requires specific gating, interacting, and dynamics properties mainly operated by a bipartite outer membrane channel called secretin. W...

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Autores principales:	Badreddine Douzi, Nhung T. T. Trinh, Sandra Michel-Souzy, Aline Desmyter, Geneviève Ball, Pascale Barbier, Artemis Kosta, Eric Durand, Katrina T. Forest, Christian Cambillau, Alain Roussel, Romé Voulhoux
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pseudomonas aeruginosa secretin dynamics protein structure-function stoichiometry type II secretion system Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bf8f42205505467f8798d46d021e96ac
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spelling	oai:doaj.org-article:bf8f42205505467f8798d46d021e96ac2021-11-15T15:51:51ZUnraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics10.1128/mBio.01185-172150-7511https://doaj.org/article/bf8f42205505467f8798d46d021e96ac2017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01185-17https://doaj.org/toc/2150-7511ABSTRACT The type II secretion system (T2SS) releases large folded exoproteins across the envelope of many Gram-negative pathogens. This secretion process therefore requires specific gating, interacting, and dynamics properties mainly operated by a bipartite outer membrane channel called secretin. We have a good understanding of the structure-function relationship of the pore-forming C-terminal domain of secretins. In contrast, the high flexibility of their periplasmic N-terminal domain has been an obstacle in obtaining the detailed structural information required to uncover its molecular function. In Pseudomonas aeruginosa, the Xcp T2SS plays an important role in bacterial virulence by its capacity to deliver a large panel of toxins and degradative enzymes into the surrounding environment. Here, we revealed that the N-terminal domain of XcpQ secretin spontaneously self-assembled into a hexamer of dimers independently of its C-terminal domain. Furthermore, and by using multidisciplinary approaches, we elucidate the structural organization of the XcpQ N domain and demonstrate that secretin flexibility at interdimer interfaces is mandatory for its function. IMPORTANCE Bacterial secretins are large homooligomeric proteins constituting the outer membrane pore-forming element of several envelope-embedded nanomachines essential in bacterial survival and pathogenicity. They comprise a well-defined membrane-embedded C-terminal domain and a modular periplasmic N-terminal domain involved in substrate recruitment and connection with inner membrane components. We are studying the XcpQ secretin of the T2SS present in the pathogenic bacterium Pseudomonas aeruginosa. Our data highlight the ability of the XcpQ N-terminal domain to spontaneously oligomerize into a hexamer of dimers. Further in vivo experiments revealed that this domain adopts different conformations essential for the T2SS secretion process. These findings provide new insights into the functional understanding of bacterial T2SS secretins.Badreddine DouziNhung T. T. TrinhSandra Michel-SouzyAline DesmyterGeneviève BallPascale BarbierArtemis KostaEric DurandKatrina T. ForestChristian CambillauAlain RousselRomé VoulhouxAmerican Society for MicrobiologyarticlePseudomonas aeruginosasecretindynamicsprotein structure-functionstoichiometrytype II secretion systemMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa secretin dynamics protein structure-function stoichiometry type II secretion system Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa secretin dynamics protein structure-function stoichiometry type II secretion system Microbiology QR1-502 Badreddine Douzi Nhung T. T. Trinh Sandra Michel-Souzy Aline Desmyter Geneviève Ball Pascale Barbier Artemis Kosta Eric Durand Katrina T. Forest Christian Cambillau Alain Roussel Romé Voulhoux Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
description	ABSTRACT The type II secretion system (T2SS) releases large folded exoproteins across the envelope of many Gram-negative pathogens. This secretion process therefore requires specific gating, interacting, and dynamics properties mainly operated by a bipartite outer membrane channel called secretin. We have a good understanding of the structure-function relationship of the pore-forming C-terminal domain of secretins. In contrast, the high flexibility of their periplasmic N-terminal domain has been an obstacle in obtaining the detailed structural information required to uncover its molecular function. In Pseudomonas aeruginosa, the Xcp T2SS plays an important role in bacterial virulence by its capacity to deliver a large panel of toxins and degradative enzymes into the surrounding environment. Here, we revealed that the N-terminal domain of XcpQ secretin spontaneously self-assembled into a hexamer of dimers independently of its C-terminal domain. Furthermore, and by using multidisciplinary approaches, we elucidate the structural organization of the XcpQ N domain and demonstrate that secretin flexibility at interdimer interfaces is mandatory for its function. IMPORTANCE Bacterial secretins are large homooligomeric proteins constituting the outer membrane pore-forming element of several envelope-embedded nanomachines essential in bacterial survival and pathogenicity. They comprise a well-defined membrane-embedded C-terminal domain and a modular periplasmic N-terminal domain involved in substrate recruitment and connection with inner membrane components. We are studying the XcpQ secretin of the T2SS present in the pathogenic bacterium Pseudomonas aeruginosa. Our data highlight the ability of the XcpQ N-terminal domain to spontaneously oligomerize into a hexamer of dimers. Further in vivo experiments revealed that this domain adopts different conformations essential for the T2SS secretion process. These findings provide new insights into the functional understanding of bacterial T2SS secretins.
format	article
author	Badreddine Douzi Nhung T. T. Trinh Sandra Michel-Souzy Aline Desmyter Geneviève Ball Pascale Barbier Artemis Kosta Eric Durand Katrina T. Forest Christian Cambillau Alain Roussel Romé Voulhoux
author_facet	Badreddine Douzi Nhung T. T. Trinh Sandra Michel-Souzy Aline Desmyter Geneviève Ball Pascale Barbier Artemis Kosta Eric Durand Katrina T. Forest Christian Cambillau Alain Roussel Romé Voulhoux
author_sort	Badreddine Douzi
title	Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
title_short	Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
title_full	Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
title_fullStr	Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
title_full_unstemmed	Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics
title_sort	unraveling the self-assembly of the <italic toggle="yes">pseudomonas aeruginosa</italic> xcpq secretin periplasmic domain provides new molecular insights into type ii secretion system secreton architecture and dynamics
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/bf8f42205505467f8798d46d021e96ac
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Unraveling the Self-Assembly of the <italic toggle="yes">Pseudomonas aeruginosa</italic> XcpQ Secretin Periplasmic Domain Provides New Molecular Insights into Type II Secretion System Secreton Architecture and Dynamics

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