Direct Measurements of the Outer Membrane Stage of Ferric Enterobactin Transport
Open accessAbstract
When Gram-negative bacteria acquire iron, the metal crosses both the outer membrane (OM) and the inner membrane, but existing radioisotopic uptake assays only measure its passage through the latter bilayer, as the accumulation of the radionuclide in the cytoplasm. We devised a methodology that exclusively observes OM transport and used it to study the uptake of ferric enterobactin (FeEnt) by Escherichia coli FepA. This technique, called postuptake binding, revealed previously unknown aspects of TonB-dependent transport reactions. The experiments showed, for the first time, that despite the discrepancy in cell envelope concentrations of FepA and TonB ( approximately 35:1), all FepA proteins were active and equivalent in FeEnt uptake, with a maximum turnover number of approximately 5/min. FepA-mediated transport of FeEnt progressed through three distinct phases with successively decreasing rates, and from its temperature dependence, the activation energy of the OM stage was 33-35 kcal/mol. The accumulation of FeEnt in the periplasm required the binding protein and inner membrane permease components of its overall transport system; postuptake binding assays on strains devoid of FepB, FepD, or FepG did not show uptake of FeEnt through the OM. However, fluorescence labeling data implied that FepA was active in the DeltafepB strain, suggesting that FeEnt entered the periplasm but then leaked out. Further experiments confirmed this futile cycle; cells without FepB transported FeEnt across the OM, but it immediately escaped through TolC.
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After reaching binding equilibrium in the surface vestibule, interactions between TonB C-terminus and FepA N-terminus induce a conformational change in the receptor that results in internalization of the iron complex into the periplasm.
“After reaching binding equilibrium in the surface vestibule, interactions between the TonB C-terminus and the FepA N-terminus induce a conformational change in the receptor that results in the internalization of the iron complex into the periplasm ( Bradbeer, 1993 ; Newton et al., 2010 ; Klebba, 2016 ).”
From Specificity and mechanism of TonB-dependent ferric catecholate uptake by Fiu (2024) · cites this paper as Newton et al., 2010
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Self-citation
- Authors
- Newton, S. M., Trinh, V., Pi, H., & Klebba, P. E.
- Affiliations
- University of Oklahoma (US)
- Corresponding author
- Klebba, Phillip E.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2010-06
- Volume
- 285
- Issue
- 23
- Pages
- 17488-17497
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2878513
- OpenAlex
- W2133716242
- Cited by
- 38
- References
- 68
- Citations by year
- 2026: 2 · 2024: 4 · 2023: 1 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 2 · 2017: 4 · 2016: 5 · 2014: 3 · 2013: 4 · 2012: 3
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0417694)
- National Institutes of Health
- National Institute of General Medical Sciences (GM 53836, R01GM053836)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- outer membrane transport, TonB-dependent transport, FepA, Escherichia coli, iron acquisition, FePd, TolC, futile cycle, activation energy, turnover number
- MeSH terms
- Bacterial Outer Membrane Proteins, Biological Transport, Carrier Proteins, Enterobactin, Escherichia coli, Iron, Kinetics, Models, Biological, Models, Chemical, Protein Binding, Receptors, Cell Surface, Periplasm, Membrane Transport Proteins, Immunoprecipitation
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