A Di- and Tripeptide Transport System Can Supply Listeria Monocytogenes Scott A with Amino Acids Essential for Growth

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 1995 Jan 1

PMID 7887604

Citations 21

Authors

A Verheul

A Hagting

M R Amezaga

I R Booth

F M Rombouts

T Abee

Affiliations

Soon will be listed here.

Abstract

Listeria monocytogenes takes up di- and tripeptides via a proton motive force-dependent carrier protein. This peptide transport system resembles the recently cloned and sequenced secondary di- and tripeptide transport system of Lactococcus lactis (A. Hagting, E. R. S. Kunji, K. J. Leenhouts, B. Poolman, and W. N. Konings, J. Biol. Chem. 269:11391-11399, 1994). The peptide permease of L. monocytogenes has a broad substrate specificity and allows transport of the nonpeptide substrate 5-aminolevulinic acid, the toxic di- and tripeptide analogs, alanyl-beta-chloroalanine and alanyl-alanyl-beta-chloroalanine, and various di- and tripeptides. No extracellular peptide hydrolysis was detected, indicating that peptides are hydrolyzed after being transported into the cell. Indeed, peptidase activities in response to various synthetic substrates were detected in cell extracts obtained from L. monocytogenes cells grown in brain heart infusion broth or defined medium. The di- and tripeptide permease can supply L. monocytogenes with essential amino acids for growth and might contribute to growth of this pathogen in various foods where peptides are supplied by proteolytic activity of other microorganisms present in these foods. Possible roles of this di- and tripeptide transport system in the osmoregulation and virulence of L. monocytogenes are discussed.

Citing Articles

cell-to-cell spread bypasses nutrient limitation for replicating intracellular bacteria.

Radhakrishnan P, Theriot J bioRxiv. 2025; .

PMID: 39975404 PMC: 11838505. DOI: 10.1101/2025.01.31.635960.

Two Permeases Associated with the Multifunctional CtaP Cysteine Transport System in Listeria monocytogenes Play Distinct Roles in Pathogenesis.

Vaval Taylor D, Xayarath B, Freitag N Microbiol Spectr. 2023; 11(3):e0331722.

PMID: 37199604 PMC: 10269559. DOI: 10.1128/spectrum.03317-22.

Synthesis and Antimicrobial Activity of Phosphonopeptide Derivatives Incorporating Single and Dual Inhibitors.

Ng K, Perry J, Marrs E, Orenga S, Anderson R, Gray M Molecules. 2020; 25(7).

PMID: 32231126 PMC: 7180716. DOI: 10.3390/molecules25071557.

Metabolism of the Gram-Positive Bacterial Pathogen .

Sauer J, Herskovits A, ORiordan M Microbiol Spectr. 2019; 7(4).

PMID: 31418407 PMC: 6699642. DOI: 10.1128/microbiolspec.GPP3-0066-2019.

Comparative Genomic Analysis of Two Serotype 1/2b Isolates from Analogous Environmental Niches Demonstrates the Influence of Hypervariable Hotspots in Defining Pathogenesis.

Casey A, Jordan K, Coffey A, Fox E, McAuliffe O Front Nutr. 2017; 3:54.

PMID: 28066772 PMC: 5174086. DOI: 10.3389/fnut.2016.00054.

References

AMES G, Mimura C, Shyamala V . Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: Traffic ATPases. FEMS Microbiol Rev. 1990; 6(4):429-46. DOI: 10.1111/j.1574-6968.1990.tb04110.x. View

Shinbo T, Kamo N, Kurihara K, Kobatake Y . A PVC-based electrode sensitive to DDA+ as a device for monitoring the membrane potential in biological systems. Arch Biochem Biophys. 1978; 187(2):414-22. DOI: 10.1016/0003-9861(78)90052-8. View

Perego M, Higgins C, Pearce S, Gallagher M, Hoch J . The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol. 1991; 5(1):173-85. DOI: 10.1111/j.1365-2958.1991.tb01838.x. View

Hugenholtz J, Splint R, Konings W, Veldkamp H . Selection of Protease-Positive and Protease-Negative Variants of Streptococcus cremoris. Appl Environ Microbiol. 1987; 53(2):309-14. PMC: 203657. DOI: 10.1128/aem.53.2.309-314.1987. View

Elliott T . Transport of 5-aminolevulinic acid by the dipeptide permease in Salmonella typhimurium. J Bacteriol. 1993; 175(2):325-31. PMC: 196145. DOI: 10.1128/jb.175.2.325-331.1993. View

Raveneau J, Geoffroy C, Beretti J, Gaillard J, ALOUF J, Berche P . Reduced virulence of a Listeria monocytogenes phospholipase-deficient mutant obtained by transposon insertion into the zinc metalloprotease gene. Infect Immun. 1992; 60(3):916-21. PMC: 257573. DOI: 10.1128/iai.60.3.916-921.1992. View

Manson M, Blank V, Brade G, Higgins C . Peptide chemotaxis in E. coli involves the Tap signal transducer and the dipeptide permease. Nature. 1986; 321(6067):253-6. DOI: 10.1038/321253a0. View

Tynkkynen S, Buist G, Kunji E, Kok J, Poolman B, Venema G . Genetic and biochemical characterization of the oligopeptide transport system of Lactococcus lactis. J Bacteriol. 1993; 175(23):7523-32. PMC: 206908. DOI: 10.1128/jb.175.23.7523-7532.1993. View

Mathiopoulos C, Mueller J, Slack F, Murphy C, Patankar S, Bukusoglu G . A Bacillus subtilis dipeptide transport system expressed early during sporulation. Mol Microbiol. 1991; 5(8):1903-13. DOI: 10.1111/j.1365-2958.1991.tb00814.x. View

10.

Domann E, Goebel W, Chakraborty T . Molecular cloning, sequencing, and identification of a metalloprotease gene from Listeria monocytogenes that is species specific and physically linked to the listeriolysin gene. Infect Immun. 1991; 59(1):65-72. PMC: 257706. DOI: 10.1128/iai.59.1.65-72.1991. View

11.

Manning J, Merrifield N, Jones W, Gotschlich E . Inhibition of bacterial growth by beta-chloro-D-alanine. Proc Natl Acad Sci U S A. 1974; 71(2):417-21. PMC: 388017. DOI: 10.1073/pnas.71.2.417. View

12.

Tam R, Saier Jr M . Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev. 1993; 57(2):320-46. PMC: 372912. DOI: 10.1128/mr.57.2.320-346.1993. View

13.

Alloing G, Trombe M, Claverys J . The ami locus of the gram-positive bacterium Streptococcus pneumoniae is similar to binding protein-dependent transport operons of gram-negative bacteria. Mol Microbiol. 1990; 4(4):633-44. DOI: 10.1111/j.1365-2958.1990.tb00632.x. View

14.

Perrett D, Webb J, Silk D, Clark M . The assay of dipeptides using fluorescamine and its application to determining dipeptidase activity. Anal Biochem. 1975; 68(1):161-6. DOI: 10.1016/0003-2697(75)90690-9. View

15.

Mengaud J, Geoffroy C, Cossart P . Identification of a new operon involved in Listeria monocytogenes virulence: its first gene encodes a protein homologous to bacterial metalloproteases. Infect Immun. 1991; 59(3):1043-9. PMC: 258365. DOI: 10.1128/iai.59.3.1043-1049.1991. View

16.

Payne J, Smith M . Peptide transport by micro-organisms. Adv Microb Physiol. 1994; 36:1-80. DOI: 10.1016/s0065-2911(08)60176-9. View

17.

Goodell E, Higgins C . Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. J Bacteriol. 1987; 169(8):3861-5. PMC: 212484. DOI: 10.1128/jb.169.8.3861-3865.1987. View

18.

Vazquez-Boland J, Kocks C, Dramsi S, Ohayon H, Geoffroy C, Mengaud J . Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun. 1992; 60(1):219-30. PMC: 257526. DOI: 10.1128/iai.60.1.219-230.1992. View

19.

MONTIE T . Chemotaxis to oligopeptides by Pseudomonas aeruginosa. Appl Environ Microbiol. 1994; 60(1):363-7. PMC: 201315. DOI: 10.1128/aem.60.1.363-367.1994. View

20.

Premaratne R, Lin W, Johnson E . Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol. 1991; 57(10):3046-8. PMC: 183920. DOI: 10.1128/aem.57.10.3046-3048.1991. View