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Microbiology 148 (2002), 1171-1182
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Microbiology (2002), 148, 1171-1182.
© 2002 Society for General Microbiology

Research Paper

Envelope instability in DNA adenine methylase mutants of Salmonella enterica

M. Graciela Pucciarelli1, Ana I. Prieto2, Josep Casadesús2 and Francisco García-del Portillo1

Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CSIC), Campus de Cantoblanco, 28049 Madrid, Spain1
Departamento de Genética, Facultad de Biología, Universidad de Sevilla, 41080 Sevilla, Spain2

Author for correspondence: Francisco García-del Portillo. Tel: +34 91 5854923. Fax: +34 91 5854506. e-mail: fgportillo{at}cnb.uam.es

Mutants of Salmonella enterica serovar Typhimurium lacking DNA adenine (Dam) methylase show reduced secretion of invasion effectors encoded in the Salmonella-pathogenicity island 1 (SPI-1). Concomitant with this alteration, a high number and quantity of extracellular proteins are detected in cultures of Dam- mutants. This study shows by subcellular fractionation analysis that the presence of numerous extracellular proteins in cultures of Dam- mutants is linked to an exacerbated release of membrane particulate material. The membrane ‘leaky’ phenotype and the impaired functionality of type III secretion systems were, however, unrelated since exacerbated release of proteins to the medium was evident in Dam- strains carrying mutations in either SPI-1 (invA, invJ) or flagellar (flhD) genes. This result supports the view that Dam methylation controls a plethora of cellular processes. Electron microscopy analysis demonstrated that the accumulation of membrane particulate material occurs preferentially as vesicles in stationary cultures of Dam- strains. In addition, a reduction in the relative amount of peptidoglycan-associated lipoprotein (PAL), TolB, OmpA and murein lipoprotein (Lpp) bound to peptidoglycan was observed in actively growing Dam- mutants. The existence of an envelope defect was further confirmed by the increased sensitivity to deoxycholate exhibited by Dam- mutants, mostly during exponential growth. Unexpectedly, lack of Dam methylation neither increased envelope instability nor impaired the association of PAL-Tol-Lpp proteins to the peptidoglycan in Escherichia coli. Accordingly, E. coli Dam- mutants did not show sensitivity to deoxycholate. Altogether, these results indicate that, besides its role in modulating the secretion of effectors by the SPI-1-encoded type III apparatus, Dam methylation controls cell envelope integrity in S. enterica.

Keywords: Dam methylation, membrane vesicle, protein secretion

Abbreviations: Dam, DNA adenine methylase; PAL, peptidoglycan-associated lipoprotein; PG, peptidoglycan (fraction); SP, secreted protein; SPI-1, Salmonella-pathogenicity island 1; TP, total protein; VES, vesicle; VSN, vesicle supernatant




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