Localized incorporation of outer membrane components in the pathogen Brucella abortus

Victoria Vassen; Claire Valotteau; Cécile Feuillie; Cécile Formosa-Dague; Yves F Dufrêne; Xavier De Bolle

doi:10.15252/embj.2018100323

Localized incorporation of outer membrane components in the pathogen Brucella abortus

Victoria Vassen
, Claire Valotteau
, Cécile Feuillie
, Cécile Formosa-Dague
, Yves F Dufrêne
, Xavier De Bolle

Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

Résumé

The zoonotic pathogen Brucella abortus is part of the Rhizobiales, which are alpha-proteobacteria displaying unipolar growth. Here, we show that this bacterium exhibits heterogeneity in its outer membrane composition, with clusters of rough lipopolysaccharide co-localizing with the essential outer membrane porin Omp2b, which is proposed to allow facilitated diffusion of solutes through the porin. We also show that the major outer membrane protein Omp25 and peptidoglycan are incorporated at the new pole and the division site, the expected growth sites. Interestingly, lipopolysaccharide is also inserted at the same growth sites. The absence of long-range diffusion of main components of the outer membrane could explain the apparent immobility of the Omp2b clusters, as well as unipolar and mid-cell localizations of newly incorporated outer membrane proteins and lipopolysaccharide. Unipolar growth and limited mobility of surface structures also suggest that new surface variants could arise in a few generations without the need of diluting pre-existing surface antigens.

langue originale	Anglais
Numéro d'article	e100323
journal	The EMBO journal
Volume	38
Numéro de publication	5
Date de mise en ligne précoce	2019
Les DOIs	https://doi.org/10.15252/embj.2018100323
Etat de la publication	Publié - 1 mars 2019

Financement

We thank Ignacio Moriy?n, Raquel Conde ?lvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-Fran?ois Collet for stimulating and helpful discussion. We thank St?phane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank K?vin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B.?abortus ?omp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the F?d?ration Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.unamur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Universit? Catholique de Louvain was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communaut? Fran?aise de Belgique (Concerted Research Action). Y.F. Dufr?ne is a Research Director at FNRS. We thank Ignacio Moriyón, Raquel Conde Álvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-François Collet for stimulating and helpful discussion. We thank Stéphane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank Kévin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B. abortus Δomp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the Fédération Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.un amur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Université Catholique de Louvain was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communauté Française de Belgique (Concerted Research Action). Y.F. Dufrêne is a Research Director at FNRS.

Bailleurs de fonds	Numéro du bailleur de fonds
fran?aise de Belgique
European Union's Horizon 2020 research and innovation program
Communauté française de Belgique
FNRS-WELBIO
HADA
Boris Vauzeilles
European Research Council
Fonds pour la Formation à la Recherche dans l'Industrie et l'Agriculture
Fédération Wallonie-Bruxelles
F?d?ration Wallonie-Bruxelles
Institut National des Sciences de l'Univers, Centre National de la Recherche Scientifique
Fonds De La Recherche Scientifique - FNRS	CDR J.0091.14, PDR T.0053.13, WELBIO-CR-2015A-05
Horizon 2020 Framework Programme	693630
Concerted Research Actions	17/22-087

Accès au document

10.15252/embj.2018100323

Autres fichiers et liens

Link to publication in Scopus

PDR (FRSM) BRUCELL-CYCLE: BRUCELL-CYCLE
De Bolle, X. (Responsable du Projet), Willemart, K. (Technicien) & ONG, T. A. P. (Chercheur)
31/12/14 → …
Projet: Recherche

Laboratoire de sécurité biologique au niveau 3 (BL3)
De Bolle, X. (!!Manager)
Plateforme technologique Laboratoire de securite biologique au niveau 3
Equipement/installations: Plateforme technolgique

Contient cette citation

@article{70f92623f7584cf4a484df2a7bb520bb,

title = "Localized incorporation of outer membrane components in the pathogen Brucella abortus",

abstract = "The zoonotic pathogen Brucella abortus is part of the Rhizobiales, which are alpha-proteobacteria displaying unipolar growth. Here, we show that this bacterium exhibits heterogeneity in its outer membrane composition, with clusters of rough lipopolysaccharide co-localizing with the essential outer membrane porin Omp2b, which is proposed to allow facilitated diffusion of solutes through the porin. We also show that the major outer membrane protein Omp25 and peptidoglycan are incorporated at the new pole and the division site, the expected growth sites. Interestingly, lipopolysaccharide is also inserted at the same growth sites. The absence of long-range diffusion of main components of the outer membrane could explain the apparent immobility of the Omp2b clusters, as well as unipolar and mid-cell localizations of newly incorporated outer membrane proteins and lipopolysaccharide. Unipolar growth and limited mobility of surface structures also suggest that new surface variants could arise in a few generations without the need of diluting pre-existing surface antigens.",

keywords = "Brucella, lipopolysaccharide, outer membrane, unipolar growth",

author = "Victoria Vassen and Claire Valotteau and C{\'e}cile Feuillie and C{\'e}cile Formosa-Dague and Dufr{\^e}ne, \{Yves F\} and \{De Bolle\}, Xavier",

note = "Funding Information: We thank Ignacio Moriy{\'o}n, Raquel Conde {\'A}lvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-Fran{\c c}ois Collet for stimulating and helpful discussion. We thank St{\'e}phane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank K{\'e}vin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B. abortus Δomp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the F{\'e}d{\'e}ration Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.un amur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Universit{\'e} Catholique de Louvain was supported by the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communaut{\'e} Fran{\c c}aise de Belgique (Concerted Research Action). Y.F. Dufr{\^e}ne is a Research Director at FNRS. Funding Information: We thank Ignacio Moriy?n, Raquel Conde ?lvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-Fran?ois Collet for stimulating and helpful discussion. We thank St?phane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank K?vin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B.?abortus ?omp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the F?d?ration Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.unamur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Universit? Catholique de Louvain was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communaut? Fran?aise de Belgique (Concerted Research Action). Y.F. Dufr?ne is a Research Director at FNRS. Publisher Copyright: {\textcopyright} 2019 The Authors Copyright: Copyright 2019 Elsevier B.V., All rights reserved.",

year = "2019",

month = mar,

day = "1",

doi = "10.15252/embj.2018100323",

language = "English",

volume = "38",

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T1 - Localized incorporation of outer membrane components in the pathogen Brucella abortus

AU - Vassen, Victoria

AU - Valotteau, Claire

AU - Feuillie, Cécile

AU - Formosa-Dague, Cécile

AU - Dufrêne, Yves F

AU - De Bolle, Xavier

N1 - Funding Information: We thank Ignacio Moriyón, Raquel Conde Álvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-François Collet for stimulating and helpful discussion. We thank Stéphane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank Kévin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B. abortus Δomp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the Fédération Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.un amur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Université Catholique de Louvain was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communauté Française de Belgique (Concerted Research Action). Y.F. Dufrêne is a Research Director at FNRS. Funding Information: We thank Ignacio Moriy?n, Raquel Conde ?lvarez, Francesco Renzi, Jean-Yves Matroule, and Jean-Fran?ois Collet for stimulating and helpful discussion. We thank St?phane Vincent and his team for the synthesis of HADA and Boris Vauzeilles for providing Kdo-N3. We thank K?vin Willemart for the technical assistance in flow cytometry and Beatriz Izquierdo Lafuente for providing the B.?abortus ?omp25 strain. This research has been funded by grants from Fonds de la Recherche Scientifique-Fonds National de la Recherche Scientifique (FRS-FNRS, http://www.fnrs.be) (PDR T.0053.13 and PDR Brucell-cycle T.0060.15, and CDR J.0091.14) to X. De Bolle. The work was also funded by a grant from Concerted Research Actions (17/22-087) of the F?d?ration Wallonie-Bruxelles, to J.-F. Collet, P. Soumillion and X. De Bolle. We thank UNamur (https://www.unamur.be/) for financial and logistic support. V. Vassen is supported by a Ph.D. grant from FRIA (FRS-FNRS). Work at the Universit? Catholique de Louvain was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement 693630), the FRS-FNRS, the FNRS-WELBIO (grant WELBIO-CR-2015A-05), and the Research Department of the Communaut? Fran?aise de Belgique (Concerted Research Action). Y.F. Dufr?ne is a Research Director at FNRS. Publisher Copyright: © 2019 The Authors Copyright: Copyright 2019 Elsevier B.V., All rights reserved.

PY - 2019/3/1

Y1 - 2019/3/1

N2 - The zoonotic pathogen Brucella abortus is part of the Rhizobiales, which are alpha-proteobacteria displaying unipolar growth. Here, we show that this bacterium exhibits heterogeneity in its outer membrane composition, with clusters of rough lipopolysaccharide co-localizing with the essential outer membrane porin Omp2b, which is proposed to allow facilitated diffusion of solutes through the porin. We also show that the major outer membrane protein Omp25 and peptidoglycan are incorporated at the new pole and the division site, the expected growth sites. Interestingly, lipopolysaccharide is also inserted at the same growth sites. The absence of long-range diffusion of main components of the outer membrane could explain the apparent immobility of the Omp2b clusters, as well as unipolar and mid-cell localizations of newly incorporated outer membrane proteins and lipopolysaccharide. Unipolar growth and limited mobility of surface structures also suggest that new surface variants could arise in a few generations without the need of diluting pre-existing surface antigens.

AB - The zoonotic pathogen Brucella abortus is part of the Rhizobiales, which are alpha-proteobacteria displaying unipolar growth. Here, we show that this bacterium exhibits heterogeneity in its outer membrane composition, with clusters of rough lipopolysaccharide co-localizing with the essential outer membrane porin Omp2b, which is proposed to allow facilitated diffusion of solutes through the porin. We also show that the major outer membrane protein Omp25 and peptidoglycan are incorporated at the new pole and the division site, the expected growth sites. Interestingly, lipopolysaccharide is also inserted at the same growth sites. The absence of long-range diffusion of main components of the outer membrane could explain the apparent immobility of the Omp2b clusters, as well as unipolar and mid-cell localizations of newly incorporated outer membrane proteins and lipopolysaccharide. Unipolar growth and limited mobility of surface structures also suggest that new surface variants could arise in a few generations without the need of diluting pre-existing surface antigens.

KW - Brucella

KW - lipopolysaccharide

KW - outer membrane

KW - unipolar growth

UR - https://www.scopus.com/pages/publications/85059862498

U2 - 10.15252/embj.2018100323

DO - 10.15252/embj.2018100323

M3 - Article

C2 - 30635335

SN - 0261-4189

VL - 38

JO - The EMBO journal

JF - The EMBO journal

IS - 5

M1 - e100323

ER -

Localized incorporation of outer membrane components in the pathogen Brucella abortus

Résumé

Financement

Accès au document

Autres fichiers et liens

Empreinte digitale

Projets

PDR (FRSM) BRUCELL-CYCLE: BRUCELL-CYCLE

Équipement

Laboratoire de sécurité biologique au niveau 3 (BL3)

Contient cette citation