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J. Biol. Chem., Vol. 281, Issue 17, 11464-11470, April 28, 2006

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The Ectodomain of the Viral Receptor YueB Forms a Fiber That Triggers Ejection of Bacteriophage SPP1 DNA^*

Carlos São-José¹, Sophie Lhuillier², Rudi Lurz^¶, Ronald Melki^||, Jean Lepault, Mário Almeida Santos, and Paulo Tavares³

From the Faculdade de Ciências de Lisboa, Instituto de Ciência Aplicada e Tecnologia e Departamento de Biologia Vegetal, 1749-016 Lisboa, Portugal, Unité de Virologie Moléculaire et Structurale, Unité Mixte de Recherche CNRS 2472, Unité Mixte de Recherche Institut Nationale, de la Recherche Agronomique 1157 and Institut Fédératif de Recherche 115, Bâtiment 14B, Avenue de la Terrasse, 91198 Gif-sur-Yvette cedex, France, ^¶Max-Planck-Institut für Molekulare Genetik, Ihnestrasse 73, 14195 Berlin, Germany, and ^||Laboratoire d'Enzymologie et Biochimie Structurales CNRS, Bâtiment 34, Avenue de la Terrasse, 91198 Gif-sur-Yvette cedex, France

The irreversible binding of bacteriophages to their receptor(s) in the host cell surface triggers release of the naked genome from the virion followed by transit of viral DNA to the host cell cytoplasm. We have purified, for the first time, a receptor from a Gram-positive bacterium that is active to trigger viral DNA ejection in vitro. This extracellular region ("ectodomain") of the Bacillus subtilis protein YueB (YueB780) was a 7 S elongated dimer forming a 36.5-nm-long fiber. YueB780 bound to the tail tip of bacteriophage SPP1. Although a stable receptor-phage interaction occurred between 0 and 37 °C, complete blocking of phage DNA release or partial ejection events were observed at temperatures below 15 °C. We also showed that the receptor was exposed to the B. subtilis surface. YueB differed structurally from phage receptors from Gram-negative bacteria. Its properties revealed a fiber spanning the full length of the 30-nm-thick peptidoglycan layer. The fiber is predicted to be anchored in the cell membrane through transmembrane segments. These features, highly suitable for a virus receptor in Gram-positive bacteria, are very likely shared by a large number of phage receptors.

Received for publication, December 21, 2005 , and in revised form, February 14, 2006.

^* This work was supported by Grant POCTI/BIA-MIC/57088/2004 from Fundação para a Ciência e Tecnologia (FCT, Portugal) (to C. S.-J.), by an Action Thématique et Incitative sur Programme from CNRS (France) (to P. T.), and by the program "Dynamique et Reactivité des Assemblages Biologiques." 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.

² Financed by a doctoral fellowship from the Ministère de l'Education Nationale de la Recherche et de la Technologie (France).

¹ Supported by the post-doctoral fellowship BPD/9429/2002 from FCT (Portugal). To whom correspondence may be addressed: Instituto de Ciência Aplicada e Tecnologia e Departamento de Biologia Vegetal, Faculdade de Ciências de Lisboa, Ed. ICAT, 1749-016 Lisboa, Portugal. Tel.: 351-217500000 (ext. 20151); Fax: 351-217500048; E-mail: cjsjose{at}fc.ul.pt. ³ To whom correspondence may be addressed: Unité de Virologie Moléculaire et Structurale, Unité Mixte de Recherche CNRS 2472, Unité Mixte de Recherche INRA 1157 and IFR 115, Bt. 14B, Ave. de la Terrasse, 91198 Gif-sur-Yvette cedex, France. Tel.: 331-69823860; Fax: 331-69824308; E-mail: tavares{at}vms.cnrs-gif.fr.

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