Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization

ABSTRACT Neisseria meningitidis is a leading cause of bacterial meningitis and septicemia, affecting infants and adults worldwide. N. meningitidis is also a common inhabitant of the human nasopharynx and, as such, is highly adapted to its niche. During bacteremia, N. meningitidis gains access to the...

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Autores principales:	Elena Capel, Aldert L. Zomer, Thomas Nussbaumer, Christine Bole, Brigitte Izac, Eric Frapy, Julie Meyer, Haniaa Bouzinba-Ségard, Emmanuelle Bille, Anne Jamet, Anne Cavau, Franck Letourneur, Sandrine Bourdoulous, Thomas Rattei, Xavier Nassif, Mathieu Coureuil
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/18206b351701404a886151e85e519b02
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spelling	oai:doaj.org-article:18206b351701404a886151e85e519b022021-11-15T15:50:19ZComprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization10.1128/mBio.01173-162150-7511https://doaj.org/article/18206b351701404a886151e85e519b022016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01173-16https://doaj.org/toc/2150-7511ABSTRACT Neisseria meningitidis is a leading cause of bacterial meningitis and septicemia, affecting infants and adults worldwide. N. meningitidis is also a common inhabitant of the human nasopharynx and, as such, is highly adapted to its niche. During bacteremia, N. meningitidis gains access to the blood compartment, where it adheres to endothelial cells of blood vessels and causes dramatic vascular damage. Colonization of the nasopharyngeal niche and communication with the different human cell types is a major issue of the N. meningitidis life cycle that is poorly understood. Here, highly saturated random transposon insertion libraries of N. meningitidis were engineered, and the fitness of mutations during routine growth and that of colonization of endothelial and epithelial cells in a flow device were assessed in a transposon insertion site sequencing (Tn-seq) analysis. This allowed the identification of genes essential for bacterial growth and genes specifically required for host cell colonization. In addition, after having identified the small noncoding RNAs (sRNAs) located in intergenic regions, the phenotypes associated with mutations in those sRNAs were defined. A total of 383 genes and 8 intergenic regions containing sRNA candidates were identified to be essential for growth, while 288 genes and 33 intergenic regions containing sRNA candidates were found to be specifically required for host cell colonization. IMPORTANCE Meningococcal meningitis is a common cause of meningitis in infants and adults. Neisseria meningitidis (meningococcus) is also a commensal bacterium of the nasopharynx and is carried by 3 to 30% of healthy humans. Under some unknown circumstances, N. meningitidis is able to invade the bloodstream and cause either meningitis or a fatal septicemia known as purpura fulminans. The onset of symptoms is sudden, and death can follow within hours. Although many meningococcal virulence factors have been identified, the mechanisms that allow the bacterium to switch from the commensal to pathogen state remain unknown. Therefore, we used a Tn-seq strategy coupled to high-throughput DNA sequencing technologies to find genes for proteins used by N. meningitidis to specifically colonize epithelial cells and primary brain endothelial cells. We identified 383 genes and 8 intergenic regions containing sRNAs essential for growth and 288 genes and 33 intergenic regions containing sRNAs required specifically for host cell colonization.Elena CapelAldert L. ZomerThomas NussbaumerChristine BoleBrigitte IzacEric FrapyJulie MeyerHaniaa Bouzinba-SégardEmmanuelle BilleAnne JametAnne CavauFranck LetourneurSandrine BourdoulousThomas RatteiXavier NassifMathieu CoureuilAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Elena Capel Aldert L. Zomer Thomas Nussbaumer Christine Bole Brigitte Izac Eric Frapy Julie Meyer Haniaa Bouzinba-Ségard Emmanuelle Bille Anne Jamet Anne Cavau Franck Letourneur Sandrine Bourdoulous Thomas Rattei Xavier Nassif Mathieu Coureuil Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
description	ABSTRACT Neisseria meningitidis is a leading cause of bacterial meningitis and septicemia, affecting infants and adults worldwide. N. meningitidis is also a common inhabitant of the human nasopharynx and, as such, is highly adapted to its niche. During bacteremia, N. meningitidis gains access to the blood compartment, where it adheres to endothelial cells of blood vessels and causes dramatic vascular damage. Colonization of the nasopharyngeal niche and communication with the different human cell types is a major issue of the N. meningitidis life cycle that is poorly understood. Here, highly saturated random transposon insertion libraries of N. meningitidis were engineered, and the fitness of mutations during routine growth and that of colonization of endothelial and epithelial cells in a flow device were assessed in a transposon insertion site sequencing (Tn-seq) analysis. This allowed the identification of genes essential for bacterial growth and genes specifically required for host cell colonization. In addition, after having identified the small noncoding RNAs (sRNAs) located in intergenic regions, the phenotypes associated with mutations in those sRNAs were defined. A total of 383 genes and 8 intergenic regions containing sRNA candidates were identified to be essential for growth, while 288 genes and 33 intergenic regions containing sRNA candidates were found to be specifically required for host cell colonization. IMPORTANCE Meningococcal meningitis is a common cause of meningitis in infants and adults. Neisseria meningitidis (meningococcus) is also a commensal bacterium of the nasopharynx and is carried by 3 to 30% of healthy humans. Under some unknown circumstances, N. meningitidis is able to invade the bloodstream and cause either meningitis or a fatal septicemia known as purpura fulminans. The onset of symptoms is sudden, and death can follow within hours. Although many meningococcal virulence factors have been identified, the mechanisms that allow the bacterium to switch from the commensal to pathogen state remain unknown. Therefore, we used a Tn-seq strategy coupled to high-throughput DNA sequencing technologies to find genes for proteins used by N. meningitidis to specifically colonize epithelial cells and primary brain endothelial cells. We identified 383 genes and 8 intergenic regions containing sRNAs essential for growth and 288 genes and 33 intergenic regions containing sRNAs required specifically for host cell colonization.
format	article
author	Elena Capel Aldert L. Zomer Thomas Nussbaumer Christine Bole Brigitte Izac Eric Frapy Julie Meyer Haniaa Bouzinba-Ségard Emmanuelle Bille Anne Jamet Anne Cavau Franck Letourneur Sandrine Bourdoulous Thomas Rattei Xavier Nassif Mathieu Coureuil
author_facet	Elena Capel Aldert L. Zomer Thomas Nussbaumer Christine Bole Brigitte Izac Eric Frapy Julie Meyer Haniaa Bouzinba-Ségard Emmanuelle Bille Anne Jamet Anne Cavau Franck Letourneur Sandrine Bourdoulous Thomas Rattei Xavier Nassif Mathieu Coureuil
author_sort	Elena Capel
title	Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
title_short	Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
title_full	Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
title_fullStr	Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
title_full_unstemmed	Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization
title_sort	comprehensive identification of meningococcal genes and small noncoding rnas required for host cell colonization
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/18206b351701404a886151e85e519b02
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Comprehensive Identification of Meningococcal Genes and Small Noncoding RNAs Required for Host Cell Colonization

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