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Journal of Bacteriology, May 2006, p. 3654-3663, Vol. 188, No. 10
0021-9193/06/$08.00+0     doi:10.1128/JB.188.10.3654-3663.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Flavonoid-Inducible Modifications to Rhamnan O Antigens Are Necessary for Rhizobium sp. Strain NGR234-Legume Symbioses

W. J. Broughton,^1,* M. Hanin,^1,, B. Reli,^1,, J. Kopciñska,² W. Golinowski,² . imek,³ T. Ojanen-Reuhs,³ B. Reuhs,³ C. Marie,^1,¶ H. Kobayashi,^1,|| B. Bordogna,¹ A. Le Quéré,¹ S. Jabbouri,^1,# R. Fellay,^1, X. Perret,¹ and W. J. Deakin¹

LBMPS, Université de Genève, 30 quai Ernest-Ansermet, 1211 Genève 4, Switzerland,¹ Department of Botany, Faculty of Agriculture, Warsaw Agricultural University, UI Nowoursynowska 159, 02-528 Warsaw, Poland,² Whistler Center for Carbohydrate Research, Department of Food Science, Purdue University, 1160 Food Science Building, West Lafayette, Indiana 47907-1160³

Received 22 November 2005/ Accepted 20 February 2006

Rhizobium sp. strain NGR234 produces a flavonoid-inducible rhamnose-rich lipopolysaccharide (LPS) that is important for the nodulation of legumes. Many of the genes encoding the rhamnan part of the molecule lie between 87° and 110° of pNGR234a, the symbiotic plasmid of NGR234. Computational methods suggest that 5 of the 12 open reading frames (ORFs) within this arc are involved in synthesis (and subsequent polymerization) of L-rhamnose. Two others probably play roles in the transport of carbohydrates. To evaluate the function of these ORFs, we mutated a number of them and tested the ability of the mutants to nodulate a variety of legumes. At the same time, changes in the production of surface polysaccharides (particularly the rhamnan O antigen) were examined. Deletion of rmlB to wbgA and mutation in fixF abolished rhamnan synthesis. Mutation of y4gM (a member of the ATP-binding cassette transporter family) did not abolish production of the rhamnose-rich LPS but, unexpectedly, the mutant displayed a symbiotic phenotype very similar to that of strains unable to produce the rhamnan O antigen (NGRrmlB-wbgA and NGRfixF). At least two flavonoid-inducible regulatory pathways are involved in synthesis of the rhamnan O antigen. Mutation of either pathway reduces rhamnan production. Coordination of rhamnan synthesis with rhizobial release from infection threads is thus part of the symbiotic interaction.

W.J.B., M.H., and B.R. contributed equally to this work.

Present address: Institut Supérieur de Biotechnologie de Sfax, Route de Soukra Km 4, 3038 Sfax, Tunisia.

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

^¶ Present address: Laboratoire de Pharmacologie Chimique et Génétique, U640 INSERM, Faculte de Sciences Pharmaceutiques et Biologiques 4, avenue de l'Observatoire, 75270 Paris Cedex 06, France.

^|| Present address: Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139.

^# Present address: Université du Littoral, Côte d'Opale, LR2B-IBB, BP120, 62327 Boulogne sur mer Cédex, France.

Present address: Novartis Consumer Health SA, 1260 Nyon, Switzerland.