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Journal of Bacteriology, September 2005, p. 6479-6487, Vol. 187, No. 18
0021-9193/05/$08.00+0     doi:10.1128/JB.187.18.6479-6487.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Structural Characterization of a Flavonoid-Inducible Pseudomonas aeruginosa A-Band-Like O Antigen of Rhizobium sp. Strain NGR234, Required for the Formation of Nitrogen-Fixing Nodules

Bradley L. Reuhs,^1, Biserka Reli,^2,, L. Scott Forsberg,³ Corinne Marie,² Tuula Ojanen-Reuhs,¹ Samuel B. Stephens,³ Chee-Hoong Wong,^2,4, Saïd Jabbouri,^2,¶ and William J. Broughton^2*

Whistler Center for Carbohydrate Research, Department of Food Science, Purdue University, 1160 Food Science Building, West Lafayette, Indiana 47907-1160,¹ LBMPS, Université de Genève, 30 quai Ernest-Ansermet, 1211 Genève 4, Switzerland,² Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Rd., Athens, Georgia 30602,³ Pusat Penyelidikan Sains Kajihayat, Universiti Sains Malaysia, Pulau Pinang, Malaysia⁴

Received 12 April 2005/ Accepted 27 June 2005

Rhizobium (Sinorhizobium) sp. strain NGR234 contains three replicons, the smallest of which (pNGR234a) carries most symbiotic genes, including those required for nodulation and lipo-chito-oligosaccharide (Nod factor) biosynthesis. Activation of nod gene expression depends on plant-derived flavonoids, NodD transcriptional activators, and nod box promoter elements. Nod boxes NB6 and NB7 delimit six different types of genes, one of which (fixF) is essential for the formation of effective nodules on Vigna unguiculata. In vegetative culture, wild-type NGR234 produces a distinct, flavonoid-inducible lipopolysaccharide (LPS) that is not produced by the mutant (NGRfixF); this LPS is also found in nitrogen-fixing bacteroids isolated from V. unguiculata infected with NGR234. Electron microscopy showed that peribacteroid membrane formation is perturbed in nodule cells infected by the fixF mutant. LPSs were purified from free-living NGR234 cultured in the presence of apigenin. Structural analyses showed that the polysaccharide portions of these LPSs are specialized, rhamnose-containing O antigens attached to a modified core-lipid A carrier. The primary sequence of the O antigen is [-3)--L-Rhap-(1,3)--L-Rhap-(1,2)--L-Rhap-(1-]_n, and the LPS core region lacks the acidic sugars commonly associated with the antigenic outer core of LPS from noninduced cells. This rhamnan O antigen, which is absent from noninduced cells, has the same primary sequence as the A-band O antigen of Pseudomonas aeruginosa, except that it is composed of L-rhamnose rather than the D-rhamnose characteristic of the latter. It is noteworthy that A-band LPS is selectively maintained on the P. aeruginosa cell surface during chronic cystic fibrosis lung infection, where it is associated with an increased duration of infection.

Both authors contributed equally to this project.

Present address: Laboratoire de Rhumatologie, CHU Sart-Tilman, Tour de Pathologie IVeme, B23, 4000 Liège, Belgium.

Present address: 79, Road 5, Minden Heights, Pulau Pinang, Malaysia.

^¶ Present address: Université du Littoral, ULCO, LR2B-ERI002, Bassin Napoléon, BP 120, F-62327 Boulogne sur mer cedex, France.

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