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PMID: 19706478 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Study of free oligosaccharides derived from the bacterial N-glycosylation pathway.

Nothaft H, Liu X, McNally DJ, Li J, Szymanski CM

Abstract

The food-borne pathogen Campylobacter jejuni is one of the leading causes of bacterial gastroenteritis worldwide and the most frequent antecedent in neuropathies such as the Guillain-Barré and Miller Fisher syndromes. C. jejuni was demonstrated to possess an N-linked protein glycosylation pathway that adds a conserved heptasaccharide to >40 periplasmic and membrane proteins. Recently, we showed that C. jejuni also produces free heptasaccharides derived from the N-glycan pathway reminiscent of the free oligosaccharides (fOS) produced by eukaryotes. Herein, we demonstrate that C. jejuni fOS are produced in response to changes in the osmolarity of the environment and bacterial growth phase. We provide evidence showing the conserved WWDYG motif of the oligosaccharyltransferase, PglB, is necessary for fOS release into the periplasm. This report demonstrates that fOS from an N-glycosylation pathway in bacteria are potentially equivalent to osmoregulated periplasmic glucans in other Gram-negative organisms.

MeSH Terms
Campylobacter jejuni/chemistry,metabolism Glycosylation Hexosyltransferases/genetics,metabolism Mass Spectrometry Mutation/genetics Oligosaccharides/chemistry,metabolism Osmotic Pressure Periplasm/metabolism Polysaccharides/metabolism Transcription, Genetic
Chemicals
Oligosaccharides Polysaccharides Hexosyltransferases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Nothaft Harald
Institute for Biological Sciences, National Research Council, Ottawa, ON, Canada K1A 0R6.
Liu Xin
McNally David J
Li Jianjun
Szymanski Christine M
References (52)
52 references, click to expand
  1. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli.
    Science. 2002 Nov 29;298(5599):1790-3 PMID: 12459590
  2. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts.
    J Biol Chem. 1965 Sep;240(9):3685-92 PMID: 4284300
  3. Potential regulation of N-glycosylation precursor through oligosaccharide-lipid hydrolase action and glucosyltransferase-glucosidase shuttle.
    J Biol Chem. 1991 Mar 15;266(8):5311-7 PMID: 1825831
  4. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3016-21 PMID: 15703289
  5. The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks.
    Microbiology (Reading). 2004 Jun;150(Pt 6):1957-1964 PMID: 15184581
  6. Linear osmoregulated periplasmic glucans are encoded by the opgGH locus of Pseudomonas aeruginosa.
    Microbiology (Reading). 2007 Oct;153(Pt 10):3255-3263 PMID: 17906125
  7. Chemoenzymatic synthesis of glycopeptides with PglB, a bacterial oligosaccharyl transferase from Campylobacter jejuni.
    Chem Biol. 2005 Dec;12(12):1311-5 PMID: 16356848
  8. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni.
    Microbiology (Reading). 2005 Jan;151(Pt 1):233-242 PMID: 15632441
  9. Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus.
    Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5933-8 PMID: 18408158
  10. Hypoosmotic adaptation in Rhizobium meliloti requires beta-(1----2)-glucan.
    J Bacteriol. 1990 Mar;172(3):1400-8 PMID: 1689716
  11. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity.
    J Bacteriol. 2001 May;183(10):3134-41 PMID: 11325942
  12. Molecular cloning and characterization of cgs, the Brucella abortus cyclic beta(1-2) glucan synthetase gene: genetic complementation of Rhizobium meliloti ndvB and Agrobacterium tumefaciens chvB mutants.
    J Bacteriol. 1998 Sep;180(17):4392-400 PMID: 9721274
  13. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance.
    Nature. 2003 Nov 20;426(6964):306-10 PMID: 14628055
  14. Biosynthesis of the N-linked glycan in Campylobacter jejuni and addition onto protein through block transfer.
    J Bacteriol. 2006 Apr;188(7):2427-34 PMID: 16547029
  15. Brucella abortus cyclic beta-1,2-glucan mutants have reduced virulence in mice and are defective in intracellular replication in HeLa cells.
    Infect Immun. 2001 Jul;69(7):4528-35 PMID: 11401996
  16. Protein glycosylation in Campylobacter jejuni: partial suppression of pglF by mutation of pseC.
    J Bacteriol. 2007 Sep;189(18):6731-3 PMID: 17631632
  17. Systems of experimental genetics for Campylobacter species.
    Methods Enzymol. 1994;235:474-81 PMID: 8057919
  18. Functional mapping of Brucella abortus cyclic beta-1,2-glucan synthase: identification of the protein domain required for cyclization.
    J Bacteriol. 2009 Feb;191(4):1230-8 PMID: 19074375
  19. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences.
    Nature. 2000 Feb 10;403(6770):665-8 PMID: 10688204
  20. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):7088-93 PMID: 16641107
  21. Characterization of an oligosaccharide-pyrophosphodolichol pyrophosphatase activity in yeast.
    Biochem J. 1988 Oct 1;255(1):235-42 PMID: 2848504
  22. Free N-linked oligosaccharide chains: formation and degradation.
    Glycoconj J. 2006 Jul;23(5-6):291-302 PMID: 16897173
  23. Role for [corrected] Agrobacterium tumefaciens ChvA protein in export of beta-1,2-glucan.
    J Bacteriol. 1989 Mar;171(3):1609-15 PMID: 2921245
  24. Campylobacter jejuni Infections: update on emerging issues and trends.
    Clin Infect Dis. 2001 Apr 15;32(8):1201-6 PMID: 11283810
  25. Gene transfer from Escherichia coli to Campylobacter species: development of shuttle vectors for genetic analysis of Campylobacter jejuni.
    J Bacteriol. 1987 Nov;169(11):5320-3 PMID: 2822671
  26. Further studies of the role of cyclic beta-glucans in symbiosis. An NdvC mutant of Bradyrhizobium japonicum synthesizes cyclodecakis-(1-->3)-beta-glucosyl.
    Plant Physiol. 1999 Mar;119(3):1057-64 PMID: 10069844
  27. Effects of Ionic and Osmotic Strength on the Glucosyltransferase of Rhizobium meliloti Responsible for Cyclic beta-(1,2)-Glucan Biosynthesis.
    Appl Environ Microbiol. 1998 Apr;64(4):1290-7 PMID: 16349538
  28. Osmotic regulation of cyclic 1,2-beta-glucan synthesis.
    Microbiology (Reading). 2000 Jul;146 ( Pt 7):1735-1742 PMID: 10878137
  29. Definition of the bacterial N-glycosylation site consensus sequence.
    EMBO J. 2006 May 3;25(9):1957-66 PMID: 16619027
  30. Osmoregulated periplasmic glucans in Proteobacteria.
    FEMS Microbiol Lett. 2000 May 1;186(1):11-9 PMID: 10779706
  31. A Rhizobium meliloti mutant that forms ineffective pseudonodules in alfalfa produces exopolysaccharide but fails to form beta-(1----2) glucan.
    J Bacteriol. 1987 Feb;169(2):880-4 PMID: 3804979
  32. Cyclic beta-glucans of members of the family Rhizobiaceae.
    Microbiol Rev. 1994 Jun;58(2):145-61 PMID: 8078434
  33. Chronic effects of Campylobacter infection.
    Microbes Infect. 2002 Apr;4(4):399-403 PMID: 11932190
  34. Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival.
    Nat Immunol. 2005 Jun;6(6):618-25 PMID: 15880113
  35. Isolation and characterization of periplasmic cyclic beta-glucans of Azorhizobium caulinodans.
    FEMS Microbiol Lett. 2003 Oct 24;227(2):263-9 PMID: 14592718
  36. Affinity-capture tandem mass spectrometric characterization of polyprenyl-linked oligosaccharides: tool to study protein N-glycosylation pathways.
    Anal Chem. 2008 Jul 15;80(14):5468-75 PMID: 18547063
  37. The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress.
    Plant Cell. 2003 Oct;15(10):2273-84 PMID: 12972670
  38. Peptides glycosylated in the endoplasmic reticulum of yeast are subsequently deglycosylated by a soluble peptide: N-glycanase activity.
    J Biol Chem. 1998 Aug 21;273(34):21526-30 PMID: 9705282
  39. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract.
    Mol Microbiol. 2004 Apr;52(2):471-84 PMID: 15066034
  40. Release of oligomannoside-type glycans as a marker of the degradation of newly synthesized glycoproteins.
    Biochem J. 1994 Feb 15;298 ( Pt 1):135-42 PMID: 8129711
  41. Proteomic analysis of a non-virulent mutant of the phytopathogenic bacterium Erwinia chrysanthemi deficient in osmoregulated periplasmic glucans: change in protein expression is not restricted to the envelope, but affects general metabolism.
    Microbiology (Reading). 2007 Mar;153(Pt 3):760-767 PMID: 17322196
  42. Role for 2-linked-beta-D-glucan in the virulence of Agrobacterium tumefaciens.
    J Bacteriol. 1985 Oct;164(1):102-6 PMID: 4044517
  43. Campylobacter protein glycosylation affects host cell interactions.
    Infect Immun. 2002 Apr;70(4):2242-4 PMID: 11895996
  44. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA.
    J Biol Chem. 2004 May 7;279(19):20327-38 PMID: 14985343
  45. Osmosensing by bacteria: signals and membrane-based sensors.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):230-62 PMID: 10066837
  46. N-linked protein glycosylation is required for full competence in Campylobacter jejuni 81-176.
    J Bacteriol. 2004 Oct;186(19):6508-14 PMID: 15375132
  47. Mass spectrometry-based glycomics strategy for exploring N-linked glycosylation in eukaryotes and bacteria.
    Anal Chem. 2006 Sep 1;78(17):6081-7 PMID: 16944887
  48. Molecular cloning and characterization of cgt, the Brucella abortus cyclic beta-1,2-glucan transporter gene, and its role in virulence.
    Infect Immun. 2004 Apr;72(4):2263-71 PMID: 15039351
  49. Catabolism of glycan moieties of lipid intermediates leads to a single Man5GlcNAc oligosaccharide isomer: a study with permeabilized CHO cells.
    Glycobiology. 1995 Jul;5(5):483-94 PMID: 8563134
  50. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model.
    Cell. 1999 Jan 8;96(1):47-56 PMID: 9989496
  51. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni.
    J Biol Chem. 2002 Nov 8;277(45):42530-9 PMID: 12186869
  52. Stability of the Agrobacterium tumefaciens VirB10 protein is modulated by growth temperature and periplasmic osmoadaption.
    J Bacteriol. 1998 Dec;180(24):6597-606 PMID: 9852004
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-09-01
Epub
2009-00-14
Pages
15019-24
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2736414
Subset
IM
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