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J. Biol. Chem., Vol. 281, Issue 39, 28981-28992, September 29, 2006

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Structural Characterization of a K-antigen Capsular Polysaccharide Essential for Normal Symbiotic Infection in Rhizobium sp. NGR234

DELETION OF THE rkpMNO LOCUS PREVENTS SYNTHESIS OF 5,7-DIACETAMIDO-3,5,7,9-TETRADEOXY-NON-2-ULOSONIC ACID^*

Antoine J.-L. Le Quéré, William J. Deakin, Christel Schmeisser, Russell W. Carlson^¶, Wolfgang R. Streit, William J. Broughton¹, and L. Scott Forsberg^¶

From the Laboratoire de Biologie Moléculaire des Plantes Supérieures (LBMPS), Université de Genève, 1292 Genève, Switzerland, the Institut für Mikrobiologie, Universität Hamburg, 22609 Hamburg, Germany, and the ^¶Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia 30602

Many early molecular events in symbiotic infection have been documented, although factors enabling Rhizobium to progress within the plant-derived infection thread and ultimately survive within the intracellular symbiosome compartment as mature nitrogen-fixing bacteroids are poorly understood. Rhizobial surface polysaccharides (SPS), including the capsular polysaccharides (K-antigens), exist in close proximity to plant-derived membranes throughout the infection process. SPSs are essential for bacterial survival, adaptation, and as potential determinants of nodulation and/or host specificity. Relatively few studies have examined the role of K-antigens in these events. However, we constructed a mutant that lacks genes essential for the production of the K-antigen strain-specific sugar precursor, pseudaminic acid, in the broad host range Rhizobium sp. NGR234. The complete structure of the K-antigen of strain NGR234 was established, and it consists of disaccharide repeating units of glucuronic and pseudaminic acid having the structure 4)--D-glucuronic acid-(14)--5,7-diacetamido-3,5,7,9-tetradeoxy-L-glycero-L-manno-nonulosonic acid-(2. Deletion of three genes located in the rkp-3 gene cluster, rkpM, rkpN, and part of rkpO, abolished pseudaminic acid synthesis, yielding a mutant in which the strain-specific K-antigen was totally absent: other surface glycoconjugates, including the lipopolysaccharides, exopolysaccharides, and flagellin glycoprotein appeared unaffected. The NGRrkpMNO mutant was symbiotically defective, showing reduced nodulation efficiency on several legumes. K-antigen production was found to decline after rhizobia were exposed to plant flavonoids, and the decrease coincided with induction of a symbiotically active (bacteroid-specific) rhamnan-LPS, suggesting an exchange of SPS occurs during bacterial differentiation in the developing nodule.

Received for publication, December 22, 2005 , and in revised form, May 30, 2006.

^* This work was supported in part by National Institutes of Health Grant GM39583 (to R. W. C.). Financial assistance was provided by the Département de l'instruction publique du Canton de Genève, by the University of Geneva, and by the Fonds National Suisse de la Recherche Scientifique (Projects 31-63893.00 and 3100AO-104097/1). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables S1-S4 and Fig. S1.

¹ To whom correspondence should be addressed. Tel.: 41-22-379-31-08; Fax: 41-22-379-3009; E-mail: william.broughton{at}bioveg.unige.ch.

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