Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth

ABSTRACT Capnocytophaga canimorsus is known to form two kinds of cells on blood agar plates (coccoid and bacillary), evoking phase variation. When grown in coculture with animal cells these bacteria appeared only as bacilli, but in the presence of vancomycin they were round, indicating that coccoid...

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Autores principales: Francesco Renzi, Pablo Manfredi, Mélanie Dol, Jian Fu, Stéphane Vincent, Guy Richard Cornelis
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Publicado: American Society for Microbiology 2015
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spelling oai:doaj.org-article:eeb5b2f520a44d3da5cbe55d1d05d1cb2021-11-15T15:41:34ZGlycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth10.1128/mBio.02507-142150-7511https://doaj.org/article/eeb5b2f520a44d3da5cbe55d1d05d1cb2015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02507-14https://doaj.org/toc/2150-7511ABSTRACT Capnocytophaga canimorsus is known to form two kinds of cells on blood agar plates (coccoid and bacillary), evoking phase variation. When grown in coculture with animal cells these bacteria appeared only as bacilli, but in the presence of vancomycin they were round, indicating that coccoid shapes likely result from weakening of the peptidoglycan layer. Polysaccharide utilization locus 5 (PUL5) and sialidase mutant bacteria, unable to retrieve glycans from glycoproteins, grew less than wild-type bacteria and also appeared polymorphic unless GlcNAc was added, suggesting that C. canimorsus is unable to synthesize GlcNAc, an essential component of peptidoglycan. Accordingly, a genome analysis was conducted and revealed that C. canimorsus strain 5 lacks the GlmM and GlmU enzymes, which convert glucosamine into GlcNAc. Expression of the Escherichia coli GlmM together with the acetyltransferase domain of GlmU allowed PUL5 mutant bacteria to grow normally, indicating that C. canimorsus is a natural auxotroph that relies on GlcNAc harvested from the host N-glycoproteins for peptidoglycan synthesis. Mucin, a heavily O-glycosylated protein abundant in saliva, also rescued growth and the shape of PUL5 mutant bacteria. Utilization of mucin was found to depend on Muc, a Sus-like system encoded by PUL9. Contrary to all known PUL-encoded systems, Muc cleaves peptide bonds of mucin rather than glycosidic linkages. Thus, C. canimorsus has adapted to build its peptidoglycan from the glycan-rich dog's mouth glycoproteins. IMPORTANCE Capnocytophaga canimorsus is a bacterium that lives as a commensal in the dog mouth and causes severe infections in humans. In vitro, it forms two kinds of cells (coccoid and bacillary), evoking phase variation. Here, we show that cell rounding likely results from weakening of the peptidoglycan layer due to a shortage of N-acetylglucosamine (GlcNAc). C. canimorsus cannot synthesize GlcNAc because of the lack of key enzymes. In its niche, the dog mouth, C. canimorsus retrieves GlcNAc by foraging glycans from salivary mucin and N-linked glycoproteins through two different apparatuses, Muc and Gpd, both of which are related to the Bacteroides starch utilization system. The Muc system is peculiar in the sense that the enzyme of the complex is a protease and not a glycosylhydrolase, as it cleaves peptide bonds in order to capture glycan chains. This study provides a molecular genetic demonstration for the complex adaptation of C. canimorsus to its ecological niche, the oral cavity of dogs.Francesco RenziPablo ManfrediMélanie DolJian FuStéphane VincentGuy Richard CornelisAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Francesco Renzi
Pablo Manfredi
Mélanie Dol
Jian Fu
Stéphane Vincent
Guy Richard Cornelis
Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
description ABSTRACT Capnocytophaga canimorsus is known to form two kinds of cells on blood agar plates (coccoid and bacillary), evoking phase variation. When grown in coculture with animal cells these bacteria appeared only as bacilli, but in the presence of vancomycin they were round, indicating that coccoid shapes likely result from weakening of the peptidoglycan layer. Polysaccharide utilization locus 5 (PUL5) and sialidase mutant bacteria, unable to retrieve glycans from glycoproteins, grew less than wild-type bacteria and also appeared polymorphic unless GlcNAc was added, suggesting that C. canimorsus is unable to synthesize GlcNAc, an essential component of peptidoglycan. Accordingly, a genome analysis was conducted and revealed that C. canimorsus strain 5 lacks the GlmM and GlmU enzymes, which convert glucosamine into GlcNAc. Expression of the Escherichia coli GlmM together with the acetyltransferase domain of GlmU allowed PUL5 mutant bacteria to grow normally, indicating that C. canimorsus is a natural auxotroph that relies on GlcNAc harvested from the host N-glycoproteins for peptidoglycan synthesis. Mucin, a heavily O-glycosylated protein abundant in saliva, also rescued growth and the shape of PUL5 mutant bacteria. Utilization of mucin was found to depend on Muc, a Sus-like system encoded by PUL9. Contrary to all known PUL-encoded systems, Muc cleaves peptide bonds of mucin rather than glycosidic linkages. Thus, C. canimorsus has adapted to build its peptidoglycan from the glycan-rich dog's mouth glycoproteins. IMPORTANCE Capnocytophaga canimorsus is a bacterium that lives as a commensal in the dog mouth and causes severe infections in humans. In vitro, it forms two kinds of cells (coccoid and bacillary), evoking phase variation. Here, we show that cell rounding likely results from weakening of the peptidoglycan layer due to a shortage of N-acetylglucosamine (GlcNAc). C. canimorsus cannot synthesize GlcNAc because of the lack of key enzymes. In its niche, the dog mouth, C. canimorsus retrieves GlcNAc by foraging glycans from salivary mucin and N-linked glycoproteins through two different apparatuses, Muc and Gpd, both of which are related to the Bacteroides starch utilization system. The Muc system is peculiar in the sense that the enzyme of the complex is a protease and not a glycosylhydrolase, as it cleaves peptide bonds in order to capture glycan chains. This study provides a molecular genetic demonstration for the complex adaptation of C. canimorsus to its ecological niche, the oral cavity of dogs.
format article
author Francesco Renzi
Pablo Manfredi
Mélanie Dol
Jian Fu
Stéphane Vincent
Guy Richard Cornelis
author_facet Francesco Renzi
Pablo Manfredi
Mélanie Dol
Jian Fu
Stéphane Vincent
Guy Richard Cornelis
author_sort Francesco Renzi
title Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
title_short Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
title_full Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
title_fullStr Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
title_full_unstemmed Glycan-Foraging Systems Reveal the Adaptation of <named-content content-type="genus-species">Capnocytophaga canimorsus</named-content> to the Dog Mouth
title_sort glycan-foraging systems reveal the adaptation of <named-content content-type="genus-species">capnocytophaga canimorsus</named-content> to the dog mouth
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/eeb5b2f520a44d3da5cbe55d1d05d1cb
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