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Journal of Bacteriology, January 2001, p. 426-434, Vol. 183, No. 2
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.2.426-434.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Identification of the nik Gene Cluster of Brucella suis: Regulation and Contribution to Urease Activity

Véronique Jubier-Maurin,1,* Agnès Rodrigue,2 Safia Ouahrani-Bettache,1 Marion Layssac,1 Marie-Andrée Mandrand-Berthelot,2 Stephan Köhler,1 and Jean-Pierre Liautard1

Institut National de la Santé et de la Recherche Médicale U-431, Institut E. Bataillon, Université Montpellier II, 34095 Montpellier,1 and Unité de Microbiologie et Génétique CNRS ERS 2009, INSA, 69621 Villeurbanne Cedex,2 France

Received 26 July 2000/Accepted 19 October 2000

Analysis of a Brucella suis 1330 gene fused to a gfp reporter, and identified as being induced in J774 murine macrophage-like cells, allowed the isolation of a gene homologous to nikA, the first gene of the Escherichia coli operon encoding the specific transport system for nickel. DNA sequence analysis of the corresponding B. suis nik locus showed that it was highly similar to that of E. coli except for localization of the nikR regulatory gene, which lies upstream from the structural nikABCDE genes and in the opposite orientation. Protein sequence comparisons suggested that the deduced nikABCDE gene products belong to a periplasmic binding protein-dependent transport system. The nikA promoter-gfp fusion was activated in vitro by low oxygen tension and metal ion deficiency and was repressed by NiCl2 excess. Insertional inactivation of nikA strongly reduced the activity of the nickel metalloenzyme urease, which was restored by addition of a nickel excess. Moreover, the nikA mutant of B. suis was functionally complemented with the E. coli nik gene cluster, leading to the recovery of urease activity. Reciprocally, an E. coli strain harboring a deleted nik operon recovered hydrogenase activity by heterologous complementation with the B. suis nik locus. Taking into account these results, we propose that the nik locus of B. suis encodes a nickel transport system. The results further suggest that nickel could enter B. suis via other transport systems. Intracellular growth rates of the B. suis wild-type and nikA mutant strains in human monocytes were similar, indicating that nikA was not essential for this step of infection. We discuss a possible role of nickel transport in maintaining enzymatic activities which could be crucial for survival of the bacteria under the environmental conditions encountered within the host.

* Corresponding author. Mailing address: INSERM U-431, Université Montpellier II, Place E. Bataillon, CC100, 34095 Montpellier Cedex 05, France. Phone: (33) 4 67 14 42 38. Fax: (33) 4 67 14 33 38. E-mail: v-maurin{at}crit.univ-montp2.fr.

Journal of Bacteriology, January 2001, p. 426-434, Vol. 183, No. 2
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.2.426-434.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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