Abstract
Chromosomally mediated AmpC-type beta-lactamases are frequently found among Enterobacteriaceae. Hyperproduction of AmpC beta-lactamase results in high-level resistance to beta-lactam antibiotics. One striking feature of Salmonella is the absence of the structural ampC gene, encoding AmpC beta-lactamase, in contrast with other members in the Enterobacteriaceae family, such as Escherichia, Citrobacter, or Enterobacter. The horizontal acquisition of ampC genes is one of the causes of the increased resistance to extended-spectrum cephalosporins and beta-lactamase inhibitors among gram-negative rods. Nevertheless, despite the high number of beta-lactam-resistant Salmonella isolates so far described, only two strains expressing resistance to cephalosporin and beta-lactamase inhibitors which is mediated by AmpC-type enzymes have been found. In this work, data are provided which support the possibility that the maintenance and expression of the ampC gene may represent an unbearable cost for Salmonella in terms of reduction of some of its lifestyle attributes, such as growth rate and invasiveness. The deleterious AmpC burden can be eliminated by decreasing the production of AmpC when both the regulatory gene, ampR, and ampC are present in Salmonella. Thus, it is suggested that the two genes have to be acquired together by Salmonella, leading to an inducible beta-lactam resistance phenotype. AmpC synthesis did not produce major variations in the peptidoglycan composition of Salmonella.
MeSH Terms
Animals
Bacterial Proteins
Cell Division/physiology
Colony Count, Microbial
Culture Media/pharmacology
Detergents/pharmacology
Mice
Octoxynol/pharmacology
Peptidoglycan/analysis
Salmonella enterica/cytology,enzymology,metabolism,physiology
Serologic Tests
Serotyping
beta-Lactamases/biosynthesis,metabolism,physiology
Chemicals
Bacterial Proteins
Culture Media
Detergents
Peptidoglycan
Octoxynol
AmpC beta-lactamases
beta-Lactamases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Morosini M I
Servicio de Microbiología, Hospital Ramón y Cajal, Madrid, Spain.
Ayala J A
Baquero F
Martínez J L
Blázquez J
References (32)
32 references, click to expand
-
Initiation of translation makes attenuation of ampC in E. coli dependent on growth rate.
Mol Gen Genet. 1985;198(3):411-5
PMID: 3892227
-
Characterization of beta-lactamases.
Antimicrob Agents Chemother. 1989 Mar;33(3):259-63
PMID: 2658779
-
Evolution and dissemination of beta-lactamases accelerated by generations of beta-lactam antibiotics.
Clin Infect Dis. 1997 Jan;24 Suppl 1:S19-45
PMID: 8994778
-
Molecular archaeology of the Escherichia coli genome.
Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9413-7
PMID: 9689094
-
Genetic map of Salmonella typhimurium, edition VIII.
Microbiol Rev. 1995 Jun;59(2):241-303
PMID: 7603411
-
Salmonella typhimurium LT2 strains which are r- m+ for all three chromosomally located systems of DNA restriction and modification.
J Bacteriol. 1983 Oct;156(1):471-4
PMID: 6352690
-
An extended-spectrum AmpC-type beta-lactamase obtained by in vitro antibiotic selection.
FEMS Microbiol Lett. 1998 Aug 1;165(1):85-90
PMID: 9711843
-
A functional classification scheme for beta-lactamases and its correlation with molecular structure.
Antimicrob Agents Chemother. 1995 Jun;39(6):1211-33
PMID: 7574506
-
Coordinate regulation of murein peptidase activity and AmpC beta-lactamase synthesis in Escherichia coli.
FEBS Lett. 1992 Jun 15;304(2-3):103-8
PMID: 1618308
-
Comparison of the overlapping frd and ampC operons of Escherichia coli with the corresponding DNA sequences in other gram-negative bacteria.
J Bacteriol. 1983 Sep;155(3):1297-305
PMID: 6350266
-
Single amino acid replacements at positions altered in naturally occurring extended-spectrum TEM beta-lactamases.
Antimicrob Agents Chemother. 1995 Jan;39(1):145-9
PMID: 7695296
-
Inducible cephalosporinase production in clinical isolates of Enterobacter cloacae is controlled by a regulatory gene that has been deleted from Escherichia coli.
EMBO J. 1986 Dec 20;5(13):3709-14
PMID: 3030737
-
The E. coli beta-lactamase attenuator mediates growth rate-dependent regulation.
Nature. 1981 Mar 19;290(5803):221-5
PMID: 7010184
-
The biological cost of antibiotic resistance.
Curr Opin Microbiol. 1999 Oct;2(5):489-93
PMID: 10508723
-
Methodology for the study of beta-lactamases.
Antimicrob Agents Chemother. 1986 Jul;30(1):6-10
PMID: 3530125
-
Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution.
Mol Microbiol. 1997 Mar;23(6):1089-97
PMID: 9106201
-
The composition of the murein of Escherichia coli.
J Biol Chem. 1988 Jul 25;263(21):10088-95
PMID: 3292521
-
Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines.
Nature. 1981 May 21;291(5812):238-9
PMID: 7015147
-
Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9.
Gene. 1986;41(2-3):337-42
PMID: 3011607
-
Ecology and speciation.
Trends Ecol Evol. 1998 Dec 1;13(12):502-6
PMID: 21238408
-
Protein measurement with the Folin phenol reagent.
J Biol Chem. 1951 Nov;193(1):265-75
PMID: 14907713
-
A plasmid-mediated CMY-2 beta-lactamase from an Algerian clinical isolate of Salmonella senftenberg.
FEMS Microbiol Lett. 1997 Jul 15;152(2):255-60
PMID: 9231418
-
Novel transferable beta-lactam resistance with cephalosporinase characteristics in Salmonella enteritidis.
J Antimicrob Chemother. 1997 Jan;39(1):85-7
PMID: 9044032
-
Cytosolic intermediates for cell wall biosynthesis and degradation control inducible beta-lactam resistance in gram-negative bacteria.
Cell. 1997 Mar 21;88(6):823-32
PMID: 9118225
-
A237T as a modulating mutation in naturally occurring extended-spectrum TEM-type beta-lactamases.
Antimicrob Agents Chemother. 1998 May;42(5):1042-4
PMID: 9593123
-
Virulence of antibiotic-resistant Salmonella typhimurium.
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3949-53
PMID: 9520473
-
Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture.
J Bacteriol. 1985 Jan;161(1):238-42
PMID: 3881387
-
Intracellular replication is essential for the virulence of Salmonella typhimurium.
Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11470-4
PMID: 1763061
-
"Black holes" and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli.
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3943-8
PMID: 9520472
-
How Salmonella became a pathogen.
Trends Microbiol. 1997 Sep;5(9):343-9
PMID: 9294889
-
Complementation of growth defect in an ampC deletion mutant of Escherichia coli.
FEMS Microbiol Lett. 1993 Dec 15;114(3):349-54
PMID: 8288112
-
Peptidoglycan structure of Salmonella typhimurium growing within cultured mammalian cells.
Mol Microbiol. 1997 Feb;23(4):693-704
PMID: 9157241