This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Elkins, C. A.
Right arrow Articles by Mullis, L. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Elkins, C. A.
Right arrow Articles by Mullis, L. B.
Agricola
Right arrow Articles by Elkins, C. A.
Right arrow Articles by Mullis, L. B.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, December 2004, p. 7200-7209, Vol. 70, No. 12
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.12.7200-7209.2004

Bile-Mediated Aminoglycoside Sensitivity in Lactobacillus Species Likely Results from Increased Membrane Permeability Attributable to Cholic Acid

Christopher A. Elkins* and Lisa B. Mullis

Division of Microbiology, National Center for Toxicological Research, United States Food and Drug Administration, Jefferson, Arkansas

Received 27 April 2004/ Accepted 20 July 2004

Few studies have been conducted on antimicrobial resistance in lactobacilli, presumably because of their nonpathogenic nature as anaerobic commensals. We assessed resistance in 43 type strains and isolates representing 14 species by using agar disk diffusion and MIC analysis in MRS medium. Most noteworthy were two general phenotypes displayed by nearly every strain tested: (i) they were more susceptible (up to 256-fold in some cases) to the deconjugated bile acid cholic acid than to the conjugate taurocholic or taurodeoxycholic acid, and (ii) they became susceptible to aminoglycosides when assayed on agar medium containing 0.5% fractionated bovine bile (ox gall). Two-dimensional MIC analyses of one representative strain, Lactobacillus plantarum WCFS1, at increasing concentrations of ox gall (0 to 30.3 mg/ml) displayed corresponding decreases in resistance to all of the aminoglycosides tested and ethidium bromide. This effect was clinically relevant, with the gentamicin MIC decreasing from >1,000 to 4 µg/ml in just 3.8 mg of ox gall per ml. In uptake studies at pH 6.5, [G-3H]gentamicin accumulation increased over control levels when cells of this strain were exposed to bile acids or reserpine but not when they were exposed to carbonyl cyanide m-chlorophenylhydrazone. The effect was dramatic, particularly with cholic acid, increasing up to 18-fold, whereas only modest increases, 3- and 5-fold, could be achieved with taurocholic acid and ox gall, respectively. Since L. plantarum, particularly strain WCFS1, is known to encode bile salt hydrolase (deconjugation) activity, our data indicate that mainly cholic acid, but not taurocholic acid, effectively permeabilizes the membrane to aminoglycosides. However, at pHs approaching neutral conditions in the intestinal lumen, aminoglycoside resistance due to membrane impermeability may be complemented by a potential efflux mechanism.

* Corresponding author. Mailing address: Division of Microbiology, National Center for Toxicological Research, 3900 NCTR Dr., Jefferson, AR 72079-9502. Phone: (870) 543-7547. Fax: (870) 543-7307. E-mail: chris.elkins{at}fda.hhs.gov.

Applied and Environmental Microbiology, December 2004, p. 7200-7209, Vol. 70, No. 12
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.12.7200-7209.2004




This article has been cited by other articles:

  • Pfeiler, E. A., Klaenhammer, T. R. (2009). Role of Transporter Proteins in Bile Tolerance of Lactobacillus acidophilus. Appl. Environ. Microbiol. 75: 6013-6016 [Abstract] [Full Text]  
  • Elkins, C. A., Mullis, L. B. (2007). Substrate Competition Studies Using Whole-Cell Accumulation Assays with the Major Tripartite Multidrug Efflux Pumps of Escherichia coli. Antimicrob. Agents Chemother. 51: 923-929 [Abstract] [Full Text]  
  • Hummel, A. S., Hertel, C., Holzapfel, W. H., Franz, C. M. A. P. (2007). Antibiotic Resistances of Starter and Probiotic Strains of Lactic Acid Bacteria. Appl. Environ. Microbiol. 73: 730-739 [Abstract] [Full Text]  
  • Eckert, R., Brady, K. M., Greenberg, E. P., Qi, F., Yarbrough, D. K., He, J., McHardy, I., Anderson, M. H., Shi, W. (2006). Enhancement of Antimicrobial Activity against Pseudomonas aeruginosa by Coadministration of G10KHc and Tobramycin. Antimicrob. Agents Chemother. 50: 3833-3838 [Abstract] [Full Text]  
  • Kurdi, P., Kawanishi, K., Mizutani, K., Yokota, A. (2006). Mechanism of growth inhibition by free bile acids in lactobacilli and bifidobacteria.. J. Bacteriol. 188: 1979-1986 [Abstract] [Full Text]  
  • Elkins, C. A., Mullis, L. B. (2006). Mammalian Steroid Hormones Are Substrates for the Major RND- and MFS-Type Tripartite Multidrug Efflux Pumps of Escherichia coli. J. Bacteriol. 188: 1191-1195 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»