The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection

ABSTRACT N-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 previousl...

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Autores principales:	Alice Boulanger, Claudine Zischek, Martine Lautier, Stevie Jamet, Pauline Rival, Sébastien Carrère, Matthieu Arlat, Emmanuelle Lauber
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/700be056350446f78d748f2dd502bbc3
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spelling	oai:doaj.org-article:700be056350446f78d748f2dd502bbc32021-11-15T15:45:54ZThe Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection10.1128/mBio.01527-142150-7511https://doaj.org/article/700be056350446f78d748f2dd502bbc32014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01527-14https://doaj.org/toc/2150-7511ABSTRACT N-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. IMPORTANCE Despite 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.Alice BoulangerClaudine ZischekMartine LautierStevie JametPauline RivalSébastien CarrèreMatthieu ArlatEmmanuelle LauberAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Alice Boulanger Claudine Zischek Martine Lautier Stevie Jamet Pauline Rival Sébastien Carrère Matthieu Arlat Emmanuelle Lauber The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
description	ABSTRACT N-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. IMPORTANCE Despite 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.
format	article
author	Alice Boulanger Claudine Zischek Martine Lautier Stevie Jamet Pauline Rival Sébastien Carrère Matthieu Arlat Emmanuelle Lauber
author_facet	Alice Boulanger Claudine Zischek Martine Lautier Stevie Jamet Pauline Rival Sébastien Carrère Matthieu Arlat Emmanuelle Lauber
author_sort	Alice Boulanger
title	The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
title_short	The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
title_full	The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
title_fullStr	The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
title_full_unstemmed	The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection
title_sort	plant pathogen <named-content content-type="genus-species">xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> exploits <italic toggle="yes">n</italic>-acetylglucosamine during infection
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/700be056350446f78d748f2dd502bbc3
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The Plant Pathogen <named-content content-type="genus-species">Xanthomonas campestris</named-content> pv. <italic toggle="yes">campestris</italic> Exploits <italic toggle="yes">N</italic>-Acetylglucosamine during Infection

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