ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>

ABSTRACT Microbes use directed motility to colonize harsh and dynamic environments. We discovered that Helicobacter pylori strains establish bacterial colonies deep in the gastric glands and identified a novel protein, ChePep, necessary to colonize this niche. ChePep is preferentially localized to t...

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Autores principales:	Michael R. Howitt, Josephine Y. Lee, Paphavee Lertsethtakarn, Roger Vogelmann, Lydia-Marie Joubert, Karen M. Ottemann, Manuel R. Amieva
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/021d0e8526b64a478198114376b676d2
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spelling	oai:doaj.org-article:021d0e8526b64a478198114376b676d22021-11-15T15:38:45ZChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>10.1128/mBio.00098-112150-7511https://doaj.org/article/021d0e8526b64a478198114376b676d22011-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00098-11https://doaj.org/toc/2150-7511ABSTRACT Microbes use directed motility to colonize harsh and dynamic environments. We discovered that Helicobacter pylori strains establish bacterial colonies deep in the gastric glands and identified a novel protein, ChePep, necessary to colonize this niche. ChePep is preferentially localized to the flagellar pole. Although mutants lacking ChePep have normal flagellar ultrastructure and are motile, they have a slight defect in swarming ability. By tracking the movement of single bacteria, we found that ∆ChePep mutants cannot control the rotation of their flagella and swim with abnormally frequent reversals. These mutants even sustain bursts of movement backwards with the flagella pulling the bacteria. Genetic analysis of the chemotaxis signaling pathway shows that ChePep regulates flagellar rotation through the chemotaxis system. By examining H. pylori within a microscopic pH gradient, we determined that ChePep is critical for regulating chemotactic behavior. The chePep gene is unique to the Epsilonproteobacteria but is found throughout this diverse group. We expressed ChePep from other members of the Epsilonproteobacteria, including the zoonotic pathogen Campylobacter jejuni and the deep sea hydrothermal vent inhabitant Caminibacter mediatlanticus, in H. pylori and found that ChePep is functionally conserved across this class. ChePep represents a new family of chemotaxis regulators unique to the Epsilonproteobacteria and illustrates the different strategies that microbes have evolved to control motility. IMPORTANCE Helicobacter pylori strains infect half of all humans worldwide and contribute to the development of peptic ulcers and gastric cancer. H. pylori cannot survive within the acidic lumen of the stomach and uses flagella to actively swim to and colonize the protective mucus and epithelium. The chemotaxis system allows H. pylori to navigate by regulating the rotation of its flagella. We identified a new protein, ChePep, which controls chemotaxis in H. pylori. ChePep mutants fail to colonize the gastric glands of mice and are completely outcompeted by normal H. pylori. Genes encoding ChePep are found only in the class Epsilonproteobacteria, which includes the human pathogen Campylobacter jejuni and environmental microbes like the deep-sea hydrothermal vent colonizer Caminibacter mediatlanticus, and we show that ChePep function is conserved in this class. Our study identifies a new colonization factor in H. pylori and also provides insight into the control and evolution of bacterial chemotaxis.Michael R. HowittJosephine Y. LeePaphavee LertsethtakarnRoger VogelmannLydia-Marie JoubertKaren M. OttemannManuel R. AmievaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 4 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Michael R. Howitt Josephine Y. Lee Paphavee Lertsethtakarn Roger Vogelmann Lydia-Marie Joubert Karen M. Ottemann Manuel R. Amieva ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
description	ABSTRACT Microbes use directed motility to colonize harsh and dynamic environments. We discovered that Helicobacter pylori strains establish bacterial colonies deep in the gastric glands and identified a novel protein, ChePep, necessary to colonize this niche. ChePep is preferentially localized to the flagellar pole. Although mutants lacking ChePep have normal flagellar ultrastructure and are motile, they have a slight defect in swarming ability. By tracking the movement of single bacteria, we found that ∆ChePep mutants cannot control the rotation of their flagella and swim with abnormally frequent reversals. These mutants even sustain bursts of movement backwards with the flagella pulling the bacteria. Genetic analysis of the chemotaxis signaling pathway shows that ChePep regulates flagellar rotation through the chemotaxis system. By examining H. pylori within a microscopic pH gradient, we determined that ChePep is critical for regulating chemotactic behavior. The chePep gene is unique to the Epsilonproteobacteria but is found throughout this diverse group. We expressed ChePep from other members of the Epsilonproteobacteria, including the zoonotic pathogen Campylobacter jejuni and the deep sea hydrothermal vent inhabitant Caminibacter mediatlanticus, in H. pylori and found that ChePep is functionally conserved across this class. ChePep represents a new family of chemotaxis regulators unique to the Epsilonproteobacteria and illustrates the different strategies that microbes have evolved to control motility. IMPORTANCE Helicobacter pylori strains infect half of all humans worldwide and contribute to the development of peptic ulcers and gastric cancer. H. pylori cannot survive within the acidic lumen of the stomach and uses flagella to actively swim to and colonize the protective mucus and epithelium. The chemotaxis system allows H. pylori to navigate by regulating the rotation of its flagella. We identified a new protein, ChePep, which controls chemotaxis in H. pylori. ChePep mutants fail to colonize the gastric glands of mice and are completely outcompeted by normal H. pylori. Genes encoding ChePep are found only in the class Epsilonproteobacteria, which includes the human pathogen Campylobacter jejuni and environmental microbes like the deep-sea hydrothermal vent colonizer Caminibacter mediatlanticus, and we show that ChePep function is conserved in this class. Our study identifies a new colonization factor in H. pylori and also provides insight into the control and evolution of bacterial chemotaxis.
format	article
author	Michael R. Howitt Josephine Y. Lee Paphavee Lertsethtakarn Roger Vogelmann Lydia-Marie Joubert Karen M. Ottemann Manuel R. Amieva
author_facet	Michael R. Howitt Josephine Y. Lee Paphavee Lertsethtakarn Roger Vogelmann Lydia-Marie Joubert Karen M. Ottemann Manuel R. Amieva
author_sort	Michael R. Howitt
title	ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
title_short	ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
title_full	ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
title_fullStr	ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
title_full_unstemmed	ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>
title_sort	chepep controls <named-content content-type="genus-species">helicobacter pylori</named-content> infection of the gastric glands and chemotaxis in the <italic toggle="yes">epsilonproteobacteria</italic>
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/021d0e8526b64a478198114376b676d2
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ChePep Controls <named-content content-type="genus-species">Helicobacter pylori</named-content> Infection of the Gastric Glands and Chemotaxis in the <italic toggle="yes">Epsilonproteobacteria</italic>

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