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Journal of Bacteriology, July 2000, p. 3717-3725, Vol. 182, No. 13
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Characterization of a Sinorhizobium meliloti ATP-Binding Cassette Histidine Transporter Also Involved in Betaine and Proline Uptake

Eric Boncompagni,dagger Laurence Dupont, Tam Mignot, Magne Østeräs,Dagger Annie Lambert, Marie-Christine Poggi, and Daniel Le Rudulier*

Laboratoire de Biologie Végétale et Microbiologie, CNRS ESA 6169, Faculté des Sciences Université de Nice-Sophia Antipolis, Parc Valrose, 06108 Nice Cedex, France

Received 23 December 1999/Accepted 4 April 2000

The symbiotic soil bacterium Sinorhizobium meliloti uses the compatible solutes glycine betaine and proline betaine for both protection against osmotic stress and, at low osmolarities, as an energy source. A PCR strategy based on conserved domains in components of the glycine betaine uptake systems from Escherichia coli (ProU) and Bacillus subtilis (OpuA and OpuC) allowed us to identify a highly homologous ATP-binding cassette (ABC) binding protein-dependent transporter in S. meliloti. This system was encoded by three genes (hutXWV) of an operon which also contained a fourth gene (hutH2) encoding a putative histidase, which is an enzyme involved in the first step of histidine catabolism. Site-directed mutagenesis of the gene encoding the periplasmic binding protein (hutX) and of the gene encoding the cytoplasmic ATPase (hutV) was done to study the substrate specificity of this transporter and its contribution in betaine uptake. These mutants showed a 50% reduction in high-affinity uptake of histidine, proline, and proline betaine and about a 30% reduction in low-affinity glycine betaine transport. When histidine was used as a nitrogen source, a 30% inhibition of growth was observed in hut mutants (hutX and hutH2). Expression analysis of the hut operon determined using a hutX-lacZ fusion revealed induction by histidine, but not by salt stress, suggesting this uptake system has a catabolic role rather than being involved in osmoprotection. To our knowledge, Hut is the first characterized histidine ABC transporter also involved in proline and betaine uptake.

* Corresponding author. Mailing address: Laboratoire de Biologie Végétale et Microbiologie, CNRS ESA 6169, Faculté des Sciences, Université de Nice-Sophia Antipolis, Parc Valrose, 06108 Nice Cedex, France. Phone: (33) 492 076 834. Fax: (33) 492 076 838. E-mail: leruduli{at}unice.fr.

dagger Present address: Department of Biological Sciences, Dartmouth College, Hanover, NH 03755.

Dagger Present address: Biozentrum, University of Basel, CH-4056 Basel, Switzerland.

Journal of Bacteriology, July 2000, p. 3717-3725, Vol. 182, No. 13
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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