Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration

Neisseria meningitidis is a Gram-negative bacterium that resides as a commensal in the upper respiratory tract of humans, but occasionally, it invades the host and causes sepsis and/or meningitis. The bacterium can produce eight autotransporters, seven of which have been studied to some detail. The...

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Main Authors: Jesús Andrés Arenas, Fernanda L Paganelli, Patricia Rodríguez-Castaño, Sara Cano-Crespo, Arie van der Ende, Jos MP van Putten, Jan Tommassen
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-11-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fcimb.2016.00162/full
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author Jesús Andrés Arenas
Fernanda L Paganelli
Patricia Rodríguez-Castaño
Sara Cano-Crespo
Arie van der Ende
Jos MP van Putten
Jan Tommassen
author_facet Jesús Andrés Arenas
Fernanda L Paganelli
Patricia Rodríguez-Castaño
Sara Cano-Crespo
Arie van der Ende
Jos MP van Putten
Jan Tommassen
author_sort Jesús Andrés Arenas
collection DOAJ
description Neisseria meningitidis is a Gram-negative bacterium that resides as a commensal in the upper respiratory tract of humans, but occasionally, it invades the host and causes sepsis and/or meningitis. The bacterium can produce eight autotransporters, seven of which have been studied to some detail. The remaining one, AutB, has not been characterized yet. Here, we show that the autB gene is broadly distributed among pathogenic Neisseria spp. The gene is intact in most meningococcal strains. However, its expression is prone to phase variation due to slipped-strand mispairing at AAGC repeats located within the DNA encoding the signal sequence and is switched off in the vast majority of these strains. Moreover, various genetic disruptions prevent autB expression in most of the strains in which the gene is in phase indicating a strong selection against AutB synthesis. We observed that autB is expressed in two of the strains examined and that AutB is secreted and exposed at the cell surface. Functionality assays revealed that AutB synthesis promotes biofilm formation and delays the passage of epithelial cell layers in vitro. We hypothesize that this autotransporter is produced during the colonization process only in specific niches to facilitate microcolony formation, but its synthesis is switched off probably to evade the immune system and facilitate human tissue invasion.
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spelling doaj.art-f8cb00ee025642dea7eab02cb8f119ee2022-12-21T23:59:21ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882016-11-01610.3389/fcimb.2016.00162222802Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial TransmigrationJesús Andrés Arenas0Fernanda L Paganelli1Patricia Rodríguez-Castaño2Sara Cano-Crespo3Arie van der Ende4Jos MP van Putten5Jan Tommassen6Utrecht UniversityUniversity Medical Center Utrecht,Utrecht UniversityUtrecht UniversityAcademic Medical CenterUtrecht UniversityUtrecht UniversityNeisseria meningitidis is a Gram-negative bacterium that resides as a commensal in the upper respiratory tract of humans, but occasionally, it invades the host and causes sepsis and/or meningitis. The bacterium can produce eight autotransporters, seven of which have been studied to some detail. The remaining one, AutB, has not been characterized yet. Here, we show that the autB gene is broadly distributed among pathogenic Neisseria spp. The gene is intact in most meningococcal strains. However, its expression is prone to phase variation due to slipped-strand mispairing at AAGC repeats located within the DNA encoding the signal sequence and is switched off in the vast majority of these strains. Moreover, various genetic disruptions prevent autB expression in most of the strains in which the gene is in phase indicating a strong selection against AutB synthesis. We observed that autB is expressed in two of the strains examined and that AutB is secreted and exposed at the cell surface. Functionality assays revealed that AutB synthesis promotes biofilm formation and delays the passage of epithelial cell layers in vitro. We hypothesize that this autotransporter is produced during the colonization process only in specific niches to facilitate microcolony formation, but its synthesis is switched off probably to evade the immune system and facilitate human tissue invasion.http://journal.frontiersin.org/Journal/10.3389/fcimb.2016.00162/fullBiofilmsHaemophilus influenzaeInfectionNeisseria meningitidisPathogenesisprotein secretion
spellingShingle Jesús Andrés Arenas
Fernanda L Paganelli
Patricia Rodríguez-Castaño
Sara Cano-Crespo
Arie van der Ende
Jos MP van Putten
Jan Tommassen
Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
Frontiers in Cellular and Infection Microbiology
Biofilms
Haemophilus influenzae
Infection
Neisseria meningitidis
Pathogenesis
protein secretion
title Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
title_full Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
title_fullStr Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
title_full_unstemmed Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
title_short Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
title_sort expression of the gene for autotransporter autb of neisseria meningitidis affects biofilm formation and epithelial transmigration
topic Biofilms
Haemophilus influenzae
Infection
Neisseria meningitidis
Pathogenesis
protein secretion
url http://journal.frontiersin.org/Journal/10.3389/fcimb.2016.00162/full
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