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: Arenas, Jesús, Paganelli, Fernanda L., Rodríguez-Castaño, Patricia, Cano-Crespo, Sara, van der Ende, Arie, van Putten, Jos P. M., Tommassen, Jan
Format: Online
Language:English
Published: Frontiers Media S.A. 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5118866/
id pubmed-5118866
recordtype oai_dc
spelling pubmed-51188662016-12-05 Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration Arenas, Jesús Paganelli, Fernanda L. Rodríguez-Castaño, Patricia Cano-Crespo, Sara van der Ende, Arie van Putten, Jos P. M. Tommassen, Jan Microbiology 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. Frontiers Media S.A. 2016-11-22 /pmc/articles/PMC5118866/ /pubmed/27921012 http://dx.doi.org/10.3389/fcimb.2016.00162 Text en Copyright © 2016 Arenas, Paganelli, Rodríguez-Castaño, Cano-Crespo, van der Ende, van Putten and Tommassen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Arenas, Jesús
Paganelli, Fernanda L.
Rodríguez-Castaño, Patricia
Cano-Crespo, Sara
van der Ende, Arie
van Putten, Jos P. M.
Tommassen, Jan
spellingShingle Arenas, Jesús
Paganelli, Fernanda L.
Rodríguez-Castaño, Patricia
Cano-Crespo, Sara
van der Ende, Arie
van Putten, Jos P. M.
Tommassen, Jan
Expression of the Gene for Autotransporter AutB of Neisseria meningitidis Affects Biofilm Formation and Epithelial Transmigration
author_facet Arenas, Jesús
Paganelli, Fernanda L.
Rodríguez-Castaño, Patricia
Cano-Crespo, Sara
van der Ende, Arie
van Putten, Jos P. M.
Tommassen, Jan
author_sort Arenas, Jesús
title 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_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_sort expression of the gene for autotransporter autb of neisseria meningitidis affects biofilm formation and epithelial transmigration
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.
publisher Frontiers Media S.A.
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5118866/
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