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Characterization of a Novel Quorum-Quenching Bacterial Strain, Burkholderia anthina HN-8, and Its Biocontrol Potential against Black Rot Disease Caused by Xanthomonas campestris pv. campestris.

ABSTRACT: Diffusible signal factor (DSF) is a type of cis unsaturated fatty acid, with a chemical structure of 11-methyl-2-dodecylene acid. DSF is widely conserved in a variety of Gram-negative bacterial pathogens and is involved in the regulation of pathogenic virulence. Quorum quenching (QQ) is a promising strategy for preventing and controlling quorum sensing (QS)-mediated bacterial infections by interfering with the QS system of pathogens. In this study, a novel DSF-degrading bacterium, Burkholderia anthina strain HN-8, was isolated and characterized for its degradation ability and potential biocontrol of black rot disease caused by Xanthomonas campestris pv. campestris (Xcc). The HN-8 strain exhibited superb DSF degradation activity and completely degraded 2 mM DSF within 48 h. In addition, we present the first evidence of bacterium having a metabolic pathway for the complete degradation and metabolism of DSF. Analysis of DSF metabolic products by gas chromatography-mass spectrometry led to the identification of dodecanal as the main intermediate product, revealing that DSF could be degraded via oxidation-reduction. Furthermore, application of strain HN-8 as a potent biocontrol agent was able to significantly reduce the severity of black rot disease in radishes and Chinese cabbage. Taken together, these results shed light on the QQ mechanisms of DSF, and they provide useful information showing the potential for the biocontrol of infectious diseases caused by DSF-dependent bacterial pathogens.

SUBMITTER: Ye T

PROVIDER: S-EPMC7601453 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Characterization of a Novel Quorum-Quenching Bacterial Strain, Burkholderia anthina HN-8, and Its Biocontrol Potential against Black Rot Disease Caused by Xanthomonas campestris pv. campestris.

Ye Tian T Zhang Wenping W Feng Zhixuan Z Fan Xinghui X Xu Xudan X Mishra Sandhya S Zhang Lianhui L Chen Shaohua S

Microorganisms 20200927 10

Diffusible signal factor (DSF) is a type of cis unsaturated fatty acid, with a chemical structure of 11-methyl-2-dodecylene acid. DSF is widely conserved in a variety of Gram-negative bacterial pathogens and is involved in the regulation of pathogenic virulence. Quorum quenching (QQ) is a promising strategy for preventing and controlling quorum sensing (QS)-mediated bacterial infections by interfering with the QS system of pathogens. In this study, a novel DSF-degrading bacterium, Burk ...[more]

PMID: 32992637

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Project description:UnlabelledN-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 campestris pv. campestris, the causal agent of black rot disease of Brassica plants, 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 vitro experiments showed that X. campestris pv. campestris exploits chitooligosaccharides, and there is indirect evidence that during the early stationary phase, X. campestris pv. campestris recycles bacterium-derived peptidoglycan/muropeptides. Results obtained also suggest that during plant infection and during growth in cabbage xylem sap, X. campestris pv. campestris encounters 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. campestris pv. campestris GlcNAc 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 campestris pv. campestris, the causal agent of black rot disease on Brassica, encounters and metabolizes GlcNAc in planta and 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.

Dataset Information

Characterization of a Novel Quorum-Quenching Bacterial Strain, Burkholderia anthina HN-8, and Its Biocontrol Potential against Black Rot Disease Caused by Xanthomonas campestris pv. campestris.

Publications

Characterization of a Novel Quorum-Quenching Bacterial Strain, <i>Burkholderia anthina</i> HN-8, and Its Biocontrol Potential against Black Rot Disease Caused by <i>Xanthomonas campestris</i> pv. <i>campestris</i>.

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