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J. Biol. Chem., Vol. 282, Issue 13, 9571-9580, March 30, 2007

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The xaxAB Genes Encoding a New Apoptotic Toxin from the Insect Pathogen Xenorhabdus nematophila Are Present in Plant and Human Pathogens^*

Fabienne Vigneux, Robert Zumbihl, Grégory Jubelin, Carlos Ribeiro¹, Joël Poncet, Stephen Baghdiguian^¶, Alain Givaudan², and Michel Brehélin³

From the Ecologie Microbienne des Insectes et Interactions Hôte-Pathogène, Unité Mixte de Recherche 1133, Institut National de la Recherche Agronomique-Université de Montpellier II, 34095 Montpellier, France, Unité Mixte de Recherche CNRS 5203, INSERM U661, Université de Montpellier I et II, 34094 Montpellier, France, and ^¶Institut des Sciences de l'Evolution, Unité Mixte de Recherche 5554 CNRS-Université de Montpellier II, 34095 Montpellier, France

Xenorhabdus nematophila, a member of the Enterobacteriaceae, kills many species of insects by strongly depressing the immune system and colonizing the entire body. A peptide cytotoxin has been purified from X. nematophila broth growth, and the cytolytic effect on insect immunocytes and hemolytic effect on mammalian red blood cells of this toxin have been described (Ribeiro, C., Vignes, M., and Brehélin, M. (2003) J. Biol. Chem. 278, 3030–3039). We show here that this toxin, Xenorhabdus -xenorhabdolysin (Xax), triggers apoptosis in both insect and mammalian cells. We also report the cloning and sequencing of two genes, xaxAB, encoding this toxin in X. nematophila. The expression of both genes in recombinant Escherichia coli led to the production of active cytotoxin/hemolysin. However, hemolytic activity was observed only if the two peptides were added in the appropriate order. Furthermore, we report here that inactivation of xaxAB genes in X. nematophila abolished the major cytotoxic activity present in broth growth, called C1. We also show that these genes are present in various entomopathogenic bacteria of the genera Xenorhabdus and Photorhabdus, in Pseudomonas entomophila, in the human pathogens Yersinia enterocolitica and Proteus mirabilis, and in the plant pathogen Pseudomonas syringae. This toxin cannot be classified in any known family of cytotoxins on the basis of amino acid sequences, locus organization, and activity features. It is, therefore, probably the prototype of a new family of binary toxins.

Received for publication, May 5, 2006 , and in revised form, November 9, 2006.

^* This work was supported by Institut National de la Recherche Agronomique Grants 2004 1133 01 and 2004 1133 02. 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 Figs. S1 and S2.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) DQ249320 [GenBank] .

¹ Recipient of an Organization for Economic Cooperation and Development (OECD) fellowship. Present address: Universidade dos Açores, Rua Mae de Deus, Ponta Delgada, Portugal.

² To whom correspondence may be addressed: Ecologie Microbienne des Insectes et Interactions Hôte-Pathogène, UMR 1133, INRA-UMII, Place Eugène Bataillon 34095 Montpellier, France. Tel.: 33-467-144-672; Fax: 33-467-144-679; E-mail: givaudan{at}univ-montp2.fr. ³ To whom correspondence may be addressed: Ecologie Microbienne des Insectes et Interactions Hôte-Pathogène, UMR 1133, INRA-UMII, Place Eugène Bataillon 34095 Montpellier, France. Tel.: 33-467-144-672; Fax: 33-467-144-679; E-mail: brehelin{at}univ-montp2.fr.

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