TonB-dependent Systems of Uropathogenic Escherichia Coli: Aerobactin and Heme Transport and TonB Are Required for Virulence in the Mouse

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2001 Sep 13

PMID 11553558

Citations 159

Authors

A G Torres

P Redford

R A Welch

S M Payne

Affiliations

Soon will be listed here.

Abstract

The uropathogenic Escherichia coli strain CFT073 has multiple iron acquisition systems, including heme and siderophore transporters. A tonB mutant derivative of CFT073 failed to use heme as an iron source or to utilize the siderophores enterobactin and aerobactin, indicating that transport of these compounds in CFT073 is TonB dependent. The TonB(-) derivative showed reduced virulence in a mouse model of urinary tract infection. Virulence was restored when the tonB gene was introduced on a plasmid. To determine the importance of the individual TonB-dependent iron transport systems during urinary tract infections, mutants defective in each of the CFT073 high-affinity iron transport systems were constructed and tested in the mouse model. Mouse virulence assays indicated that mutants defective in a single iron transport system were able to infect the kidney when inoculated as a pure culture but were unable to efficiently compete with the wild-type strain in mixed infections. These results indicate a role for TonB-dependent systems in the virulence of uropathogenic E. coli strains.

Citing Articles

Metaproteomics reveals diet-induced changes in gut microbiome function according to Crohn's disease location.

Mortera S, Marzano V, Rapisarda F, Marangelo C, Pirona I, Vernocchi P Microbiome. 2024; 12(1):217.

PMID: 39443987 PMC: 11515613. DOI: 10.1186/s40168-024-01927-5.

Non-classical roles of bacterial siderophores in pathogenesis.

Arnold E Front Cell Infect Microbiol. 2024; 14:1465719.

PMID: 39372500 PMC: 11449898. DOI: 10.3389/fcimb.2024.1465719.

Heme sequestration by hemophilin from reduces respiratory tract colonization and infection with non-typeable .

Fulte S, Atto B, McCarty A, Horn K, Redzic J, Eisenmesser E mSphere. 2024; 9(3):e0000624.

PMID: 38380941 PMC: 10964412. DOI: 10.1128/msphere.00006-24.

Detection and characterization of potentially hybrid enteroaggregative Escherichia coli (EAEC) strains isolated from urinary tract infection.

Moazeni S, Badouei M, Hashemitabar G, Rezatofighi S, Mahmoodi F Braz J Microbiol. 2023; 55(1):1-9.

PMID: 38036848 PMC: 10920591. DOI: 10.1007/s42770-023-01195-9.

Tunable force transduction through the cell envelope.

Williams-Jones D, Webby M, Press C, Gradon J, Armstrong S, Szczepaniak J Proc Natl Acad Sci U S A. 2023; 120(47):e2306707120.

PMID: 37972066 PMC: 10666116. DOI: 10.1073/pnas.2306707120.

References

Guyer D, Kao J, Mobley H . Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and Catheter-associated bacteriuria and from fecal samples. Infect Immun. 1998; 66(9):4411-7. PMC: 108533. DOI: 10.1128/IAI.66.9.4411-4417.1998. View

Nagy G, Dobrindt U, Kupfer M, Emody L, Karch H, Hacker J . Expression of hemin receptor molecule ChuA is influenced by RfaH in uropathogenic Escherichia coli strain 536. Infect Immun. 2001; 69(3):1924-8. PMC: 98105. DOI: 10.1128/IAI.69.3.1924-1928.2001. View

Torres A, Payne S . Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol. 1997; 23(4):825-33. DOI: 10.1046/j.1365-2958.1997.2641628.x. View

Law D, Kelly J . Use of heme and hemoglobin by Escherichia coli O157 and other Shiga-like-toxin-producing E. coli serogroups. Infect Immun. 1995; 63(2):700-2. PMC: 173054. DOI: 10.1128/iai.63.2.700-702.1995. View

Henderson D, Payne S . Vibrio cholerae iron transport systems: roles of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems. Infect Immun. 1994; 62(11):5120-5. PMC: 303233. DOI: 10.1128/iai.62.11.5120-5125.1994. View

Seliger S, Mey A, Valle A, Payne S . The two TonB systems of Vibrio cholerae: redundant and specific functions. Mol Microbiol. 2001; 39(3):801-12. DOI: 10.1046/j.1365-2958.2001.02273.x. View

Takase H, Nitanai H, Hoshino K, Otani T . Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun. 2000; 68(8):4498-504. PMC: 98358. DOI: 10.1128/IAI.68.8.4498-4504.2000. View

Runyen-Janecky L, Hong M, Payne S . The virulence plasmid-encoded impCAB operon enhances survival and induced mutagenesis in Shigella flexneri after exposure to UV radiation. Infect Immun. 1999; 67(3):1415-23. PMC: 96475. DOI: 10.1128/IAI.67.3.1415-1423.1999. View

Reeves S, Torres A, Payne S . TonB is required for intracellular growth and virulence of Shigella dysenteriae. Infect Immun. 2000; 68(11):6329-36. PMC: 97716. DOI: 10.1128/IAI.68.11.6329-6336.2000. View

10.

Braun V, Hantke K, Koster W . Bacterial iron transport: mechanisms, genetics, and regulation. Met Ions Biol Syst. 1998; 35:67-145. View

11.

Leeds J, Welch R . Enhancing transcription through the Escherichia coli hemolysin operon, hlyCABD: RfaH and upstream JUMPStart DNA sequences function together via a postinitiation mechanism. J Bacteriol. 1997; 179(11):3519-27. PMC: 179143. DOI: 10.1128/jb.179.11.3519-3527.1997. View

12.

Stojiljkovic I, Hwa V, De Saint Martin L, OGaora P, Nassif X, Heffron F . The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol Microbiol. 1995; 15(3):531-41. DOI: 10.1111/j.1365-2958.1995.tb02266.x. View

13.

Montgomerie J, Bindereif A, NEILANDS J, KALMANSON G, Guze L . Association of hydroxamate siderophore (aerobactin) with Escherichia coli isolated from patients with bacteremia. Infect Immun. 1984; 46(3):835-8. PMC: 261622. DOI: 10.1128/iai.46.3.835-838.1984. View

14.

Tsolis R, Baumler A, Heffron F, Stojiljkovic I . Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun. 1996; 64(11):4549-56. PMC: 174411. DOI: 10.1128/iai.64.11.4549-4556.1996. View

15.

Mobley H, Green D, Trifillis A, Johnson D, Chippendale G, Lockatell C . Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun. 1990; 58(5):1281-9. PMC: 258621. DOI: 10.1128/iai.58.5.1281-1289.1990. View

16.

Braun V . Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol Rev. 1995; 16(4):295-307. DOI: 10.1111/j.1574-6976.1995.tb00177.x. View

17.

Wyckoff E, Duncan D, Torres A, Mills M, Maase K, Payne S . Structure of the Shigella dysenteriae haem transport locus and its phylogenetic distribution in enteric bacteria. Mol Microbiol. 1998; 28(6):1139-52. DOI: 10.1046/j.1365-2958.1998.00873.x. View

18.

Gorbacheva V, Faundez G, Godfrey H, Cabello F . Restricted growth of ent(-) and tonB mutants of Salmonella enterica serovar Typhi in human Mono Mac 6 monocytic cells. FEMS Microbiol Lett. 2001; 196(1):7-11. DOI: 10.1111/j.1574-6968.2001.tb10532.x. View

19.

Crosa J . Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev. 1989; 53(4):517-30. PMC: 372751. DOI: 10.1128/mr.53.4.517-530.1989. View

20.

Occhino D, Wyckoff E, Henderson D, Wrona T, Payne S . Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol Microbiol. 1998; 29(6):1493-507. DOI: 10.1046/j.1365-2958.1998.01034.x. View