Peptidoglycan maturation enzymes affect flagellar functionality in bacteria
Identifieur interne : 005620 ( Main/Exploration ); précédent : 005619; suivant : 005621Peptidoglycan maturation enzymes affect flagellar functionality in bacteria
Auteurs : Sophie Roure [France] ; Mathilde Bonis [France] ; Catherine Chaput [France, Allemagne] ; Chantal Ecobichon [France] ; Austin Mattox [France] ; Charlotte Barrière [France] ; Nina Geldmacher [Allemagne] ; Stéphanie Guadagnini [France] ; Christine Schmitt [France] ; Marie-Christine Prévost [France] ; Agnès Labigne [France] ; Steffen Backert [Irlande (pays)] ; Richard L. Ferrero [France, Australie] ; Ivo G. Boneca [France]Source :
- Molecular Microbiology [ 0950-382X ] ; 2012-11.
English descriptors
- KwdEn :
- Active site, Agella, Agellar, Agellar assembly, Agellar motor, Agellin, Agellum, Assay, Average glycan chain length, Bacterial motility, Bacterium, Blackwell publishing, Chaput, Cleaving enzymes, Coli, Coli strain, Coli strains, Colonization, Colonize, Flaa, Flgj, Full motility, Functionality, Gastric, Glutamate residue, Glycan, Glycan chains, Helicobacter, Helicobacter pylori, Hpmotb, Immun, Inactivation, Independent clones, Independent experiment, Independent experiments, Institut pasteur, Isogenic, Localization, Ltgs, Lytic, Lytic transglycosylases, Microbiol, Microbiology, Mltc, Mltc mutants, Mltd, Mltd inactivation, Mltd mutants, Mltdwkm, Molecular microbiology, Mota, Motb, Motility, Motility assays, Motility halo, Mutant, Paralysed phenotype, Parental, Parental strain, Paris france, Pathogen, Peptidoglycan, Peptidoglycan maturation, Phenotype, Plasmid, Proc natl acad, Pylorus, Roure, Salmonella, Salmonella typhimurium, Several ltgs, Sltwkm, Statistical analysis, Stator, Stator functionality, Typhimurium.
- Teeft :
- Active site, Agella, Agellar, Agellar assembly, Agellar motor, Agellin, Agellum, Assay, Average glycan chain length, Bacterial motility, Bacterium, Blackwell publishing, Chaput, Cleaving enzymes, Coli, Coli strain, Coli strains, Colonization, Colonize, Flaa, Flgj, Full motility, Functionality, Gastric, Glutamate residue, Glycan, Glycan chains, Helicobacter, Helicobacter pylori, Hpmotb, Immun, Inactivation, Independent clones, Independent experiment, Independent experiments, Institut pasteur, Isogenic, Localization, Ltgs, Lytic, Lytic transglycosylases, Microbiol, Microbiology, Mltc, Mltc mutants, Mltd, Mltd inactivation, Mltd mutants, Mltdwkm, Molecular microbiology, Mota, Motb, Motility, Motility assays, Motility halo, Mutant, Paralysed phenotype, Parental, Parental strain, Paris france, Pathogen, Peptidoglycan, Peptidoglycan maturation, Phenotype, Plasmid, Proc natl acad, Pylorus, Roure, Salmonella, Salmonella typhimurium, Several ltgs, Sltwkm, Statistical analysis, Stator, Stator functionality, Typhimurium.
Abstract
The flagellar machinery is a highly complex organelle composed of a free rotating flagellum and a fixed stator that converts energy into movement. The assembly of the flagella and the stator requires interactions with the peptidoglycan layer through which the organelle has to pass for externalization. Lytic transglycosylases are peptidoglycan degrading enzymes that cleave the sugar backbone of peptidoglycan layer. We show that an endogenous lytic transglycosylase is required for full motility of Helicobacter pylori and colonization of the gastric mucosa. Deficiency of motility resulted from a paralysed phenotype implying an altered ability to generate flagellar rotation. Similarly, another Gram‐negative pathogen Salmonella typhimurium and the Gram‐positive pathogen Listeria monocytogenes required the activity of lytic transglycosylases, Slt or MltC, and a glucosaminidase (Auto), respectively, for full motility. Furthermore, we show that in absence of the appropriate lytic transglycosylase, the flagellar motor protein MotB from H. pylori does not localize properly to the bacterial pole. We present a new model involving the maturation of the surrounding peptidoglycan for the proper anchoring and functionality of the flagellar motor.
Url:
DOI: 10.1111/mmi.12019
Affiliations:
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Boneca</name><affiliation wicri:level="3"><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Group Biology and Genetics of the Bacterial Cell Wall, F‐75015, Paris</wicri:regionArea><placeName><settlement type="city">Paris</settlement><region type="région" nuts="2">Île-de-France</region></placeName></affiliation><affiliation wicri:level="3"><country xml:lang="fr">France</country><wicri:regionArea>INSERM, Groupe Avenir, F‐75015, Paris</wicri:regionArea><placeName><settlement type="city">Paris</settlement><region type="région" nuts="2">Île-de-France</region></placeName></affiliation><affiliation wicri:level="1"><country wicri:rule="url">France</country></affiliation></author></analytic><monogr></monogr><series><title level="j" type="main">Molecular Microbiology</title><title level="j" type="alt">MOLECULAR MICROBIOLOGY</title><idno type="ISSN">0950-382X</idno><idno type="eISSN">1365-2958</idno><imprint><biblScope unit="vol">86</biblScope><biblScope unit="issue">4</biblScope><biblScope unit="page" from="845">845</biblScope><biblScope unit="page" to="856">856</biblScope><biblScope unit="page-count">12</biblScope><date type="published" when="2012-11">2012-11</date></imprint><idno type="ISSN">0950-382X</idno></series></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">0950-382X</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Active site</term><term>Agella</term><term>Agellar</term><term>Agellar assembly</term><term>Agellar motor</term><term>Agellin</term><term>Agellum</term><term>Assay</term><term>Average glycan chain length</term><term>Bacterial motility</term><term>Bacterium</term><term>Blackwell publishing</term><term>Chaput</term><term>Cleaving enzymes</term><term>Coli</term><term>Coli strain</term><term>Coli strains</term><term>Colonization</term><term>Colonize</term><term>Flaa</term><term>Flgj</term><term>Full motility</term><term>Functionality</term><term>Gastric</term><term>Glutamate residue</term><term>Glycan</term><term>Glycan chains</term><term>Helicobacter</term><term>Helicobacter pylori</term><term>Hpmotb</term><term>Immun</term><term>Inactivation</term><term>Independent clones</term><term>Independent experiment</term><term>Independent experiments</term><term>Institut pasteur</term><term>Isogenic</term><term>Localization</term><term>Ltgs</term><term>Lytic</term><term>Lytic transglycosylases</term><term>Microbiol</term><term>Microbiology</term><term>Mltc</term><term>Mltc mutants</term><term>Mltd</term><term>Mltd inactivation</term><term>Mltd mutants</term><term>Mltdwkm</term><term>Molecular microbiology</term><term>Mota</term><term>Motb</term><term>Motility</term><term>Motility assays</term><term>Motility halo</term><term>Mutant</term><term>Paralysed phenotype</term><term>Parental</term><term>Parental strain</term><term>Paris france</term><term>Pathogen</term><term>Peptidoglycan</term><term>Peptidoglycan maturation</term><term>Phenotype</term><term>Plasmid</term><term>Proc natl acad</term><term>Pylorus</term><term>Roure</term><term>Salmonella</term><term>Salmonella typhimurium</term><term>Several ltgs</term><term>Sltwkm</term><term>Statistical analysis</term><term>Stator</term><term>Stator functionality</term><term>Typhimurium</term></keywords><keywords scheme="Teeft" xml:lang="en"><term>Active site</term><term>Agella</term><term>Agellar</term><term>Agellar assembly</term><term>Agellar motor</term><term>Agellin</term><term>Agellum</term><term>Assay</term><term>Average glycan chain length</term><term>Bacterial motility</term><term>Bacterium</term><term>Blackwell publishing</term><term>Chaput</term><term>Cleaving enzymes</term><term>Coli</term><term>Coli strain</term><term>Coli strains</term><term>Colonization</term><term>Colonize</term><term>Flaa</term><term>Flgj</term><term>Full motility</term><term>Functionality</term><term>Gastric</term><term>Glutamate residue</term><term>Glycan</term><term>Glycan chains</term><term>Helicobacter</term><term>Helicobacter pylori</term><term>Hpmotb</term><term>Immun</term><term>Inactivation</term><term>Independent clones</term><term>Independent experiment</term><term>Independent experiments</term><term>Institut pasteur</term><term>Isogenic</term><term>Localization</term><term>Ltgs</term><term>Lytic</term><term>Lytic transglycosylases</term><term>Microbiol</term><term>Microbiology</term><term>Mltc</term><term>Mltc mutants</term><term>Mltd</term><term>Mltd inactivation</term><term>Mltd mutants</term><term>Mltdwkm</term><term>Molecular microbiology</term><term>Mota</term><term>Motb</term><term>Motility</term><term>Motility assays</term><term>Motility halo</term><term>Mutant</term><term>Paralysed phenotype</term><term>Parental</term><term>Parental strain</term><term>Paris france</term><term>Pathogen</term><term>Peptidoglycan</term><term>Peptidoglycan maturation</term><term>Phenotype</term><term>Plasmid</term><term>Proc natl acad</term><term>Pylorus</term><term>Roure</term><term>Salmonella</term><term>Salmonella typhimurium</term><term>Several ltgs</term><term>Sltwkm</term><term>Statistical analysis</term><term>Stator</term><term>Stator functionality</term><term>Typhimurium</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract">The flagellar machinery is a highly complex organelle composed of a free rotating flagellum and a fixed stator that converts energy into movement. The assembly of the flagella and the stator requires interactions with the peptidoglycan layer through which the organelle has to pass for externalization. Lytic transglycosylases are peptidoglycan degrading enzymes that cleave the sugar backbone of peptidoglycan layer. We show that an endogenous lytic transglycosylase is required for full motility of Helicobacter pylori and colonization of the gastric mucosa. Deficiency of motility resulted from a paralysed phenotype implying an altered ability to generate flagellar rotation. Similarly, another Gram‐negative pathogen Salmonella typhimurium and the Gram‐positive pathogen Listeria monocytogenes required the activity of lytic transglycosylases, Slt or MltC, and a glucosaminidase (Auto), respectively, for full motility. Furthermore, we show that in absence of the appropriate lytic transglycosylase, the flagellar motor protein MotB from H. pylori does not localize properly to the bacterial pole. We present a new model involving the maturation of the surrounding peptidoglycan for the proper anchoring and functionality of the flagellar motor.</div></front></TEI><affiliations><list><country><li>Allemagne</li><li>Australie</li><li>France</li><li>Irlande (pays)</li></country><region><li>Berlin</li><li>Île-de-France</li></region><settlement><li>Berlin</li><li>Paris</li></settlement></list><tree><country name="France"><region name="Île-de-France"><name sortKey="Roure, Sophie" sort="Roure, Sophie" uniqKey="Roure S" first="Sophie" last="Roure">Sophie Roure</name></region><name sortKey="Barriere, Charlotte" sort="Barriere, Charlotte" uniqKey="Barriere C" first="Charlotte" last="Barrière">Charlotte Barrière</name><name sortKey="Boneca, Ivo G" sort="Boneca, Ivo G" uniqKey="Boneca I" first="Ivo G." last="Boneca">Ivo G. Boneca</name><name sortKey="Boneca, Ivo G" sort="Boneca, Ivo G" uniqKey="Boneca I" first="Ivo G." last="Boneca">Ivo G. Boneca</name><name sortKey="Boneca, Ivo G" sort="Boneca, Ivo G" uniqKey="Boneca I" first="Ivo G." last="Boneca">Ivo G. Boneca</name><name sortKey="Bonis, Mathilde" sort="Bonis, Mathilde" uniqKey="Bonis M" first="Mathilde" last="Bonis">Mathilde Bonis</name><name sortKey="Bonis, Mathilde" sort="Bonis, Mathilde" uniqKey="Bonis M" first="Mathilde" last="Bonis">Mathilde Bonis</name><name sortKey="Chaput, Catherine" sort="Chaput, Catherine" uniqKey="Chaput C" first="Catherine" last="Chaput">Catherine Chaput</name><name sortKey="Ecobichon, Chantal" sort="Ecobichon, Chantal" uniqKey="Ecobichon C" first="Chantal" last="Ecobichon">Chantal Ecobichon</name><name sortKey="Ecobichon, Chantal" sort="Ecobichon, Chantal" uniqKey="Ecobichon C" first="Chantal" last="Ecobichon">Chantal Ecobichon</name><name sortKey="Ferrero, Richard L" sort="Ferrero, Richard L" uniqKey="Ferrero R" first="Richard L." last="Ferrero">Richard L. Ferrero</name><name sortKey="Guadagnini, Stephanie" sort="Guadagnini, Stephanie" uniqKey="Guadagnini S" first="Stéphanie" last="Guadagnini">Stéphanie Guadagnini</name><name sortKey="Labigne, Agnes" sort="Labigne, Agnes" uniqKey="Labigne A" first="Agnès" last="Labigne">Agnès Labigne</name><name sortKey="Mattox, Austin" sort="Mattox, Austin" uniqKey="Mattox A" first="Austin" last="Mattox">Austin Mattox</name><name sortKey="Mattox, Austin" sort="Mattox, Austin" uniqKey="Mattox A" first="Austin" last="Mattox">Austin Mattox</name><name sortKey="Prevost, Marie Hristine" sort="Prevost, Marie Hristine" uniqKey="Prevost M" first="Marie-Christine" last="Prévost">Marie-Christine Prévost</name><name sortKey="Roure, Sophie" sort="Roure, Sophie" uniqKey="Roure S" first="Sophie" last="Roure">Sophie Roure</name><name sortKey="Schmitt, Christine" sort="Schmitt, Christine" uniqKey="Schmitt C" first="Christine" last="Schmitt">Christine Schmitt</name></country><country name="Allemagne"><region name="Berlin"><name sortKey="Chaput, Catherine" sort="Chaput, Catherine" uniqKey="Chaput C" first="Catherine" last="Chaput">Catherine Chaput</name></region><name sortKey="Geldmacher, Nina" sort="Geldmacher, Nina" uniqKey="Geldmacher N" first="Nina" last="Geldmacher">Nina Geldmacher</name></country><country name="Irlande (pays)"><noRegion><name sortKey="Backert, Steffen" sort="Backert, Steffen" uniqKey="Backert S" first="Steffen" last="Backert">Steffen Backert</name></noRegion></country><country name="Australie"><noRegion><name sortKey="Ferrero, Richard L" sort="Ferrero, Richard L" uniqKey="Ferrero R" first="Richard L." last="Ferrero">Richard L. 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