<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella

ABSTRACT Helicobacter pylori has an impressive ability to persist chronically in the human stomach. Similar characteristics are associated with biofilm formation in other bacteria. The H. pylori biofilm process, however, is poorly understood. To gain insight into this mode of growth, we carried out...

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Autores principales:	Skander Hathroubi, Julia Zerebinski, Karen M. Ottemann
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Helicobacter pylori biofilm flagella stress metabolism RNA-seq Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b50b426b331047d3af999be6e3d2124d
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spelling	oai:doaj.org-article:b50b426b331047d3af999be6e3d2124d2021-11-15T15:58:20Z<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella10.1128/mBio.01973-182150-7511https://doaj.org/article/b50b426b331047d3af999be6e3d2124d2018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01973-18https://doaj.org/toc/2150-7511ABSTRACT Helicobacter pylori has an impressive ability to persist chronically in the human stomach. Similar characteristics are associated with biofilm formation in other bacteria. The H. pylori biofilm process, however, is poorly understood. To gain insight into this mode of growth, we carried out comparative transcriptomic analysis between H. pylori biofilm and planktonic cells, using the mouse-colonizing strain SS1. Optimal biofilm formation was obtained with a low concentration of serum and 3 days of growth, conditions that caused both biofilm and planktonic cells to be ∼80% coccoid. Transcriptome sequencing (RNA-seq) analysis found that 8.18% of genes were differentially expressed between biofilm and planktonic cell transcriptomes. Biofilm-downregulated genes included those involved in metabolism and translation, suggesting these cells have low metabolic activity. Biofilm-upregulated genes included those whose products were predicted to be at the cell envelope, involved in regulating a stress response, and surprisingly, genes related to formation of the flagellar apparatus. Scanning electron microscopy visualized flagella that appeared to be a component of the biofilm matrix, supported by the observation that an aflagellated mutant displayed a less robust biofilm with no apparent filaments. We observed flagella in the biofilm matrix of additional H. pylori strains, supporting that flagellar use is widespread. Our data thus support a model in which H. pylori biofilm involves a multigene stress-biased response and that flagella play an important role in H. pylori biofilm formation. IMPORTANCE Biofilms, communities of bacteria that are embedded in a hydrated matrix of extracellular polymeric substances, pose a substantial health risk and are key contributors to many chronic and recurrent infections. Chronicity and recalcitrant infections are also common features associated with the ulcer-causing human pathogen H. pylori. However, relatively little is known about the role of biofilms in H. pylori pathogenesis, as well as the biofilm structure itself and the genes associated with this mode of growth. In the present study, we found that H. pylori biofilm cells highly expressed genes related to cell envelope and stress response, as well as those encoding the flagellar apparatus. Flagellar filaments were seen in high abundance in the biofilm. Flagella are known to play a role in initial biofilm formation, but typically are downregulated after that state. H. pylori instead appears to have coopted these structures for nonmotility roles, including a role building a robust biofilm.Skander HathroubiJulia ZerebinskiKaren M. OttemannAmerican Society for MicrobiologyarticleHelicobacter pyloribiofilmflagellastressmetabolismRNA-seqMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Helicobacter pylori biofilm flagella stress metabolism RNA-seq Microbiology QR1-502
spellingShingle	Helicobacter pylori biofilm flagella stress metabolism RNA-seq Microbiology QR1-502 Skander Hathroubi Julia Zerebinski Karen M. Ottemann <named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
description	ABSTRACT Helicobacter pylori has an impressive ability to persist chronically in the human stomach. Similar characteristics are associated with biofilm formation in other bacteria. The H. pylori biofilm process, however, is poorly understood. To gain insight into this mode of growth, we carried out comparative transcriptomic analysis between H. pylori biofilm and planktonic cells, using the mouse-colonizing strain SS1. Optimal biofilm formation was obtained with a low concentration of serum and 3 days of growth, conditions that caused both biofilm and planktonic cells to be ∼80% coccoid. Transcriptome sequencing (RNA-seq) analysis found that 8.18% of genes were differentially expressed between biofilm and planktonic cell transcriptomes. Biofilm-downregulated genes included those involved in metabolism and translation, suggesting these cells have low metabolic activity. Biofilm-upregulated genes included those whose products were predicted to be at the cell envelope, involved in regulating a stress response, and surprisingly, genes related to formation of the flagellar apparatus. Scanning electron microscopy visualized flagella that appeared to be a component of the biofilm matrix, supported by the observation that an aflagellated mutant displayed a less robust biofilm with no apparent filaments. We observed flagella in the biofilm matrix of additional H. pylori strains, supporting that flagellar use is widespread. Our data thus support a model in which H. pylori biofilm involves a multigene stress-biased response and that flagella play an important role in H. pylori biofilm formation. IMPORTANCE Biofilms, communities of bacteria that are embedded in a hydrated matrix of extracellular polymeric substances, pose a substantial health risk and are key contributors to many chronic and recurrent infections. Chronicity and recalcitrant infections are also common features associated with the ulcer-causing human pathogen H. pylori. However, relatively little is known about the role of biofilms in H. pylori pathogenesis, as well as the biofilm structure itself and the genes associated with this mode of growth. In the present study, we found that H. pylori biofilm cells highly expressed genes related to cell envelope and stress response, as well as those encoding the flagellar apparatus. Flagellar filaments were seen in high abundance in the biofilm. Flagella are known to play a role in initial biofilm formation, but typically are downregulated after that state. H. pylori instead appears to have coopted these structures for nonmotility roles, including a role building a robust biofilm.
format	article
author	Skander Hathroubi Julia Zerebinski Karen M. Ottemann
author_facet	Skander Hathroubi Julia Zerebinski Karen M. Ottemann
author_sort	Skander Hathroubi
title	<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
title_short	<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
title_full	<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
title_fullStr	<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
title_full_unstemmed	<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella
title_sort	<named-content content-type="genus-species">helicobacter pylori</named-content> biofilm involves a multigene stress-biased response, including a structural role for flagella
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/b50b426b331047d3af999be6e3d2124d
work_keys_str_mv	AT skanderhathroubi namedcontentcontenttypegenusspecieshelicobacterpylorinamedcontentbiofilminvolvesamultigenestressbiasedresponseincludingastructuralroleforflagella AT juliazerebinski namedcontentcontenttypegenusspecieshelicobacterpylorinamedcontentbiofilminvolvesamultigenestressbiasedresponseincludingastructuralroleforflagella AT karenmottemann namedcontentcontenttypegenusspecieshelicobacterpylorinamedcontentbiofilminvolvesamultigenestressbiasedresponseincludingastructuralroleforflagella
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<named-content content-type="genus-species">Helicobacter pylori</named-content> Biofilm Involves a Multigene Stress-Biased Response, Including a Structural Role for Flagella

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