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Journal of Bacteriology, June 2009, p. 3615-3622, Vol. 191, No. 11
0021-9193/09/$08.00+0     doi:10.1128/JB.01592-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Roles of the Outer Membrane Protein AsmA of Salmonella enterica in the Control of marRAB Expression and Invasion of Epithelial Cells{triangledown}

Ana I. Prieto,1,{dagger} Sara B. Hernández,1 Ignacio Cota,1 M. Graciela Pucciarelli,2,3 Yuri Orlov,1,{ddagger} Francisco Ramos-Morales,1 Francisco García-del Portillo,3 and Josep Casadesús1*

Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Apartado 1095, Seville 41080,1 Departamento de Biología Molecular, Universidad Autónoma de Madrid, Cantoblanco, 28049 Madrid,2 Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, C. S. I. C., Darwin 3, Cantoblanco, 28049 Madrid, Spain3

Received 10 November 2008/ Accepted 25 March 2009

A genetic screen for suppressors of bile sensitivity in DNA adenine methylase (dam) mutants of Salmonella enterica serovar Typhimurium yielded insertions in an uncharacterized locus homologous to the Escherichia coli asmA gene. Disruption of asmA suppressed bile sensitivity also in phoP and wec mutants of S. enterica and increased the MIC of sodium deoxycholate for the parental strain ATCC 14028. Increased levels of marA mRNA were found in asmA, asmA dam, asmA phoP, and asmA wec strains of S. enterica, suggesting that lack of AsmA activates expression of the marRAB operon. Hence, asmA mutations may enhance bile resistance by inducing gene expression changes in the marRAB-controlled Mar regulon. In silico analysis of AsmA structure predicted the existence of one transmembrane domain. Biochemical analysis of subcellular fractions revealed that the asmA gene of S. enterica encodes a protein of ~70 kDa located in the outer membrane. Because AsmA is unrelated to known transport and/or efflux systems, we propose that activation of marRAB in asmA mutants may be a consequence of envelope reorganization. Competitive infection of BALB/c mice with asmA+ and asmA isogenic strains indicated that lack of AsmA attenuates Salmonella virulence by the oral route but not by the intraperitoneal route. Furthermore, asmA mutants showed a reduced ability to invade epithelial cells in vitro.

* Corresponding author. Mailing address: Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Apartado 1095, E-41080 Seville, Spain. Phone: 34 95 455 7105. Fax: 34 95 455 7104. E-mail: casadesus{at}us.es

{triangledown} Published ahead of print on 3 April 2009.

{dagger} Present address: Department of Pathology, Cambridge University, Tennis Court Road, Cambridge CB2 1QP, England.

{ddagger} Permanent address: Biophysics Department, St. Petersburg Polytechnical University, Polytekhnicheskaya St., 195251 Saint Petersburg, Russia.

Journal of Bacteriology, June 2009, p. 3615-3622, Vol. 191, No. 11
0021-9193/09/$08.00+0     doi:10.1128/JB.01592-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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