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The Plant Pathogen Xanthomonas campestrispv. campestrisExploits N-Acetylglucosamine during Infection

Authors :
Boulanger, Alice
Zischek, Claudine
Lautier, Martine
Jamet, Stevie
Rival, Pauline
Carrère, Sébastien
Arlat, Matthieu
Lauber, Emmanuelle
Source :
mBio; September 2014, Vol. 5 Issue: 5
Publication Year :
2014

Abstract

ABSTRACTN-Acetylglucosamine (GlcNAc), the main component of chitin and a major constituent of bacterial peptidoglycan, is present only in trace amounts in plants, in contrast to the huge amount of various sugars that compose the polysaccharides of the plant cell wall. Thus, GlcNAc has not previously been considered a substrate exploited by phytopathogenic bacteria during plant infection. Xanthomonas campestrispv. campestris, the causal agent of black rot disease of Brassicaplants, expresses a carbohydrate utilization system devoted to GlcNAc exploitation. In addition to genes involved in GlcNAc catabolism, this system codes for four TonB-dependent outer membrane transporters (TBDTs) and eight glycoside hydrolases. Expression of all these genes is under the control of GlcNAc. In vitroexperiments showed that X. campestrispv. campestrisexploits chitooligosaccharides, and there is indirect evidence that during the early stationary phase, X. campestrispv. campestrisrecycles bacterium-derived peptidoglycan/muropeptides. Results obtained also suggest that during plant infection and during growth in cabbage xylem sap, X. campestrispv. campestrisencounters and metabolizes plant-derived GlcNAc-containing molecules. Specific TBDTs seem to be preferentially involved in the consumption of all these plant-, fungus- and bacterium-derived GlcNAc-containing molecules. This is the first evidence of GlcNAc consumption during infection by a phytopathogenic bacterium. Interestingly, N-glycans from plant N-glycosylated proteins are proposed to be substrates for glycoside hydrolases belonging to the X. campestrispv. campestrisGlcNAc exploitation system. This observation extends the range of sources of GlcNAc metabolized by phytopathogenic bacteria during their life cycle.IMPORTANCEDespite the central role of N-acetylglucosamine (GlcNAc) in nature, there is no evidence that phytopathogenic bacteria metabolize this compound during plant infection. Results obtained here suggest that Xanthomonas campestrispv. campestris, the causal agent of black rot disease on Brassica, encounters and metabolizes GlcNAc in plantaand in vitro. Active and specific outer membrane transporters belonging to the TonB-dependent transporters family are proposed to import GlcNAc-containing complex molecules from the host, from the bacterium, and/or from the environment, and bacterial glycoside hydrolases induced by GlcNAc participate in their degradation. Our results extend the range of sources of GlcNAc metabolized by this phytopathogenic bacterium during its life cycle to include chitooligosaccharides that could originate from fungi or insects present in the plant environment, muropeptides leached during peptidoglycan recycling and bacterial lysis, and N-glycans from plant N-glycosylated proteins present in the plant cell wall as well as in xylem sap.

Details

Language :
English
ISSN :
21612129 and 21507511
Volume :
5
Issue :
5
Database :
Supplemental Index
Journal :
mBio
Publication Type :
Periodical
Accession number :
ejs57733983
Full Text :
https://doi.org/10.1128/mBio.01527-14