Characterization of<i>Vibrio cholerae</i>O1 Antigen as the Bacteriophage K139 Receptor and Identification of IS<i>1004</i>Insertions Aborting O1 Antigen Biosynthesis

Nesper, Jutta; Kapfhammer, Dagmar; Klose, Karl E.; Merkert, Hilde; Reidl, Joachim

doi:10.1128/jb.182.18.5097-5104.2000

Cited by 58 publications

(54 citation statements)

References 52 publications

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“…However, constitutive synthesis of the same capsular polysaccharide probably would be disastrous for the organism over time in the complex intestinal ecosystem. Defensive products produced by the host, such as antibody, or offensive products produced by other members of the microbiota target surface polysaccharides (23)(24)(25). Thus, the capacity to produce multiple phase-variable capsular polysaccharides creates diverse populations with regard to surface architecture, including some that would be less susceptible to attack by deleterious products.…”

Section: Discussionmentioning

confidence: 99%

Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis

Coyne

Chatzidaki‐Livanis

Paoletti

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

103

104

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Bacteroides species are the most abundant Gram-negative bacteria of the human colonic microbiota. These endogenous organisms are unique in that they synthesize an extensive number of phase-variable surface polysaccharides. Pathogenic bacteria phase vary expression of surface molecules for immune evasion, but the importance of the synthesis of multiple phase-variable polysaccharides to these commensal bacteria is unknown. We previously showed that a Bacteroides fragilis mutant unable to synthesize 4 of the 8 capsular polysaccharides and unable to glycosylate proteins properly is rapidly outcompeted by the wild-type strain for colonization of the gnotobiotic mouse intestine. In the present study, we constructed mutants defective only in capsule polysaccharide synthesis to define better the importance of these surface molecules to intestinal colonization. We discovered a key enzymatic activity required for synthesis of 7 of the 8 capsular polysaccharides. Deletion of its gene resulted in the first B. fragilis mutant able to synthesize only one phase-variable polysaccharide, and further mutation resulted in a stable acapsular mutant. We show that the acapsular mutant is rapidly outcompeted, but synthesis of a single polysaccharide is sufficient for the organism to colonize the gnotobiotic intestine competitively. These data demonstrate that initial colonization of the gnotobiotic mouse intestine by B. fragilis requires that the organism synthesize only a single polysaccharide and suggest that the synthesis of multiple phase-variable polysaccharides is important for the bacteria's long-term maintenance in the normally complex and competitive ecosystem. acapsular ͉ microbiota ͉ phase variation ͉ polysaccharide ͉ glycoprotein T he human intestinal tract is home to a vast and diverse alliance of microbes comprising one of the densest microbial ecosystems in the world and one that provides functions essential to human health. Many species of the order Bacteroidales are abundant members of the human intestinal microbiota and have served as models for studying mutualistic bacterial-host relationships in this ecosystem (1, 2). Despite their importance, relatively little is known about the biology of the predominant members of this ecosystem. Deciphering how these mutualistic microorganisms successfully and stably colonize the human intestine may help us understand how they are tolerated, how different members interact with one another, what additional benefits the microbiota provide us, and how microbiotaassociated diseases are triggered in the susceptible host.The intestinal Bacteroidales synthesize a vast repertoire of surface glycans. A single strain of B. fragilis synthesizes 8 distinct capsular polysaccharides (3), an extracellular polysaccharide (4), and numerous glycoproteins (5). The synthesis of extensive numbers of glycosylated molecules is a general property of the intestinal Bacteroidales (6-8). We estimate that the genome of B. fragilis 9343 encodes Ϸ80 glycosyltransferases and dedicates at least 215,000 bp of ...

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Section: Discussionmentioning

confidence: 99%

Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis

Coyne

Chatzidaki‐Livanis

Paoletti

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

103

104

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“…Surface PSs are often the targets of phage adhesions (12)(13)(14), phage glycosidases (15), and host immune molecules that are deleterious to bacteria. The ability to create diverse bacterial cells each synthesizing different single surface PSs would allow the organism to evade attack from phage and potentially other factors of the intestinal milieu that target specific PSs.…”

Section: Discussionmentioning

confidence: 99%

Trans locus inhibitors limit concomitant polysaccharide synthesis in the human gut symbiont Bacteroides fragilis

Chatzidaki‐Livanis

Weinacht²,

Comstock³

2010

Proc. Natl. Acad. Sci. U.S.A.

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Bacteroides is an abundant genus of bacteria of the human intestinal microbiota. Bacteroides species synthesize a large number of capsular polysaccharides (PS), a biological property not shared with closely related oral species, suggesting importance for intestinal survival. Bacteroides fragilis, for example, synthesizes eight capsular polysaccharides per strain, each of which phase varies via inversion of the promoters located upstream of seven of the eight polysaccharide biosynthesis operons. In a single cell, many of these polysaccharide loci promoters can be simultaneously oriented on for transcription of the downstream biosynthesis operons. Here, we demonstrate that despite the promoter orientations, concomitant transcription of multiple polysaccharide loci within a cell is inhibited. The proteins encoded by the second gene of each of these eight loci, collectively designated the UpxZ proteins, inhibit the synthesis of heterologous polysaccharides. These unique proteins interfere with the ability of UpxY proteins encoded by other polysaccharide loci to function in transcriptional antitermination of their respective operon. The eight UpxZs have different inhibitory spectra, thus establishing a hierarchical regulatory network for polysaccharide synthesis. Limitation of concurrent polysaccharide synthesis strongly suggests that these bacteria evolved this property as an evasiontype mechanism to avoid killing by polysaccharide-targeting factors in the ecosystem.

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“…For a number of phages the LPS (LOS) structure or its components (Nesper et al, 2000;Kutter et al, 2005), are the phage receptor(s). It was therefore reasonable to check whether there is a difference between the LOS structure of the resistant and sensitive variant derivatives from both wild-type and dam cells.…”

Section: Changes In the Los Of H Influenzae Are Responsible For The mentioning

confidence: 99%

“…Bacterial phage receptors are present in the outermembrane proteins, or the lipopolysaccharide (LPS) (Nesper et al, 2000;Kutter et al, 2005). In H. influenzae the particular surface-exposed epitopes of LOS are subject to high-frequency PV (Hood et al, 1996a;Patrick et al, 1987;Weiser et al, 1989;Bayliss et al, 2002;De Bolle et al, 2000), as are the outer-membrane proteins (Bayliss et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection

2005

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Haemophilus influenzae uses phase variation (PV) to modulate the activity of its defence systems against phage infection. The PV of the restriction-modification (R-M) system HindI, the main defence system against phage infection and incoming chromosomal and phage DNA in H. influenzae Rd, is driven by changes of the pentanucleotide repeat tract within the coding sequence of the hsdM gene and is influenced by lack of Dam methylation. Phase-variable resistance/sensitivity to phage infection correlates with changes in lipooligosaccharide (LOS) structure and occurs by slippage of tetranucleotide repeats within the gene lic2A, coding for a step in the biosynthesis of LOS. The lack of Dam activity destabilizes the tetranuclotide (59-CAAT) repeat tract and increases the frequency of switching from sensitivity to resistance to phage infection more than in the opposite direction. The PV of the lgtC gene does not influence resistance or sensitivity to phage infection. Insertional inactivation of lic2A, but not lgtC or lgtF, leads to resistance to phage infection and to the same structure of the LOS as observed among phase-variable phage-resistant variants. This indicates that in the H. influenzae Rd LOS only the first two sugars (Glc-Gal) extending from the third heptose are part of bacterial phage receptors.

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Characterization ofVibrio choleraeO1 Antigen as the Bacteriophage K139 Receptor and Identification of IS1004Insertions Aborting O1 Antigen Biosynthesis

Cited by 58 publications

References 52 publications

Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis

Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis

Trans locus inhibitors limit concomitant polysaccharide synthesis in the human gut symbiont Bacteroides fragilis

The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection

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