Previous Article | Next Article 
Infection and Immunity, February 2005, p. 894-904, Vol. 73, No. 2
0019-9567/05/$08.00+0 doi:10.1128/IAI.73.2.894-904.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
Contribution of Three Bile-Associated Loci, bsh, pva, and btlB, to Gastrointestinal Persistence and Bile Tolerance of Listeria monocytogenes
Máire Begley,1
Roy D. Sleator,1
Cormac G. M. Gahan,1,2* and
Colin Hill1
Department of Microbiology and Alimentary Pharmabiotic Centre,1
School of Pharmacy, University College Cork, Cork, Ireland2
Received 12 May 2004/
Returned for modification 29 July 2004/
Accepted 12 October 2004
Listeria monocytogenes must resist the deleterious actions of bile in order to infect and subsequently colonize the human gastrointestinal tract. The molecular mechanisms used by the bacterium to resist bile and the influence of bile on pathogenesis are as yet largely unexplored. This study describes the analysis of three genesbsh, pva, and btlBpreviously annotated as bile-associated loci in the sequenced L. monocytogenes EGDe genome (lmo2067, lmo0446, and lmo0754, respectively). Analysis of deletion mutants revealed a role for all three genes in resisting the acute toxicity of bile and bile salts, particularly glycoconjugated bile salts at low pH. Mutants were unaffected in the other stress responses examined (acid, salt, and detergents). Bile hydrolysis assays demonstrate that L. monocytogenes possesses only one bile salt hydrolase gene, namely, bsh. Transcriptional analyses and activity assays revealed that, although it is regulated by both PrfA and
B, the latter appears to play the greater role in modulating bsh expression. In addition to being incapable of bile hydrolysis, a sigB mutant was shown to be exquisitely sensitive to bile salts. Furthermore, increased expression of sigB was detected under anaerobic conditions and during murine infection. A gene previously annotated as a possible penicillin V amidase (pva) or bile salt hydrolase was shown to be required for resistance to penicillin V but not penicillin G but did not demonstrate a role in bile hydrolysis. Finally, animal (murine) studies revealed an important role for both bsh and btlB in the intestinal persistence of L. monocytogenes.
* Corresponding author. Mailing address: Department of Microbiology, University College Cork, College Rd., Cork, Ireland. Phone: (353) 21-4901363. Fax: (353) 21-4903101. E-mail:
c.gahan{at}ucc.ie.
Editor: V. J. DiRita
Infection and Immunity, February 2005, p. 894-904, Vol. 73, No. 2
0019-9567/05/$08.00+0 doi:10.1128/IAI.73.2.894-904.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Merritt, M. E., Donaldson, J. R.
(2009). Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol
58: 1533-1541
[Abstract]
[Full Text]
-
Fang, F., Li, Y., Bumann, M., Raftis, E. J., Casey, P. G., Cooney, J. C., Walsh, M. A., O'Toole, P. W.
(2009). Allelic Variation of Bile Salt Hydrolase Genes in Lactobacillus salivarius Does Not Determine Bile Resistance Levels. J. Bacteriol.
191: 5743-5757
[Abstract]
[Full Text]
-
Sleator, R. D., Watson, D., Hill, C., Gahan, C. G. M.
(2009). The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology
155: 2463-2475
[Abstract]
[Full Text]
-
Abram, F., Starr, E., Karatzas, K. A. G., Matlawska-Wasowska, K., Boyd, A., Wiedmann, M., Boor, K. J., Connally, D., O'Byrne, C. P.
(2008). Identification of Components of the Sigma B Regulon in Listeria monocytogenes That Contribute to Acid and Salt Tolerance. Appl. Environ. Microbiol.
74: 6848-6858
[Abstract]
[Full Text]
-
Jones, B. V., Begley, M., Hill, C., Gahan, C. G. M., Marchesi, J. R.
(2008). Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. USA
105: 13580-13585
[Abstract]
[Full Text]
-
Lambert, J. M., Siezen, R. J., de Vos, W. M., Kleerebezem, M.
(2008). Improved annotation of conjugated bile acid hydrolase superfamily members in Gram-positive bacteria. Microbiology
154: 2492-2500
[Abstract]
[Full Text]
-
Azcarate-Peril, M. A., Altermann, E., Goh, Y. J., Tallon, R., Sanozky-Dawes, R. B., Pfeiler, E. A., O'Flaherty, S., Buck, B. L., Dobson, A., Duong, T., Miller, M. J., Barrangou, R., Klaenhammer, T. R.
(2008). Analysis of the Genome Sequence of Lactobacillus gasseri ATCC 33323 Reveals the Molecular Basis of an Autochthonous Intestinal Organism. Appl. Environ. Microbiol.
74: 4610-4625
[Abstract]
[Full Text]
-
Lambert, J. M., Bongers, R. S., de Vos, W. M., Kleerebezem, M.
(2008). Functional Analysis of Four Bile Salt Hydrolase and Penicillin Acylase Family Members in Lactobacillus plantarum WCFS1. Appl. Environ. Microbiol.
74: 4719-4726
[Abstract]
[Full Text]
-
Monk, I. R., Gahan, C. G. M., Hill, C.
(2008). Tools for Functional Postgenomic Analysis of Listeria monocytogenes. Appl. Environ. Microbiol.
74: 3921-3934
[Abstract]
[Full Text]
-
Abram, F., Su, W.-L., Wiedmann, M., Boor, K. J., Coote, P., Botting, C., Karatzas, K. A. G., O'Byrne, C. P.
(2008). Proteomic Analyses of a Listeria monocytogenes Mutant Lacking {sigma}B Identify New Components of the {sigma}B Regulon and Highlight a Role for {sigma}B in the Utilization of Glycerol. Appl. Environ. Microbiol.
74: 594-604
[Abstract]
[Full Text]
-
Raengpradub, S., Wiedmann, M., Boor, K. J.
(2008). Comparative Analysis of the {sigma}B-Dependent Stress Responses in Listeria monocytogenes and Listeria innocua Strains Exposed to Selected Stress Conditions. Appl. Environ. Microbiol.
74: 158-171
[Abstract]
[Full Text]
-
McGann, P., Wiedmann, M., Boor, K. J.
(2007). The Alternative Sigma Factor {sigma}B and the Virulence Gene Regulator PrfA Both Regulate Transcription of Listeria monocytogenes Internalins. Appl. Environ. Microbiol.
73: 2919-2930
[Abstract]
[Full Text]
-
Hain, T., Steinweg, C., Kuenne, C. T., Billion, A., Ghai, R., Chatterjee, S. S., Domann, E., Karst, U., Goesmann, A., Bekel, T., Bartels, D., Kaiser, O., Meyer, F., Puhler, A., Weisshaar, B., Wehland, J., Liang, C., Dandekar, T., Lampidis, R., Kreft, J., Goebel, W., Chakraborty, T.
(2006). Whole-Genome Sequence of Listeria welshimeri Reveals Common Steps in Genome Reduction with Listeria innocua as Compared to Listeria monocytogenes. J. Bacteriol.
188: 7405-7415
[Abstract]
[Full Text]
-
Kazmierczak, M. J., Wiedmann, M., Boor, K. J.
(2006). Contributions of Listeria monocytogenes {sigma}B and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology
152: 1827-1838
[Abstract]
[Full Text]
-
Gray, M. J., Freitag, N. E., Boor, K. J.
(2006). How the Bacterial Pathogen Listeria monocytogenes Mediates the Switch from Environmental Dr. Jekyll to Pathogenic Mr. Hyde.. Infect. Immun.
74: 2505-2512
[Full Text]
-
Bron, P. A., Monk, I. R., Corr, S. C., Hill, C., Gahan, C. G. M.
(2006). Novel Luciferase Reporter System for In Vitro and Organ-Specific Monitoring of Differential Gene Expression in Listeria monocytogenes. Appl. Environ. Microbiol.
72: 2876-2884
[Abstract]
[Full Text]
-
Begley, M., Hill, C., Gahan, C. G. M.
(2006). Bile salt hydrolase activity in probiotics.. Appl. Environ. Microbiol.
72: 1729-1738
[Full Text]
-
Begley, M., Hill, C., Ross, R. P.
(2006). Tolerance of Listeria monocytogenes to Cell Envelope-Acting Antimicrobial Agents Is Dependent on SigB.. Appl. Environ. Microbiol.
72: 2231-2234
[Abstract]
[Full Text]
-
Garner, M. R., Njaa, B. L., Wiedmann, M., Boor, K. J.
(2006). Sigma B Contributes to Listeria monocytogenes Gastrointestinal Infection but Not to Systemic Spread in the Guinea Pig Infection Model. Infect. Immun.
74: 876-886
[Abstract]
[Full Text]
-
Chatterjee, S. S., Hossain, H., Otten, S., Kuenne, C., Kuchmina, K., Machata, S., Domann, E., Chakraborty, T., Hain, T.
(2006). Intracellular Gene Expression Profile of Listeria monocytogenes. Infect. Immun.
74: 1323-1338
[Abstract]
[Full Text]
-
Rea, R., Hill, C., Gahan, C. G. M.
(2005). Listeria monocytogenes PerR Mutants Display a Small-Colony Phenotype, Increased Sensitivity to Hydrogen Peroxide, and Significantly Reduced Murine Virulence. Appl. Environ. Microbiol.
71: 8314-8322
[Abstract]
[Full Text]