The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
Biosynthesis and IroC‐dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium
Abstract
In response to iron deprivation, Salmonella enterica serovar Typhimurium secretes two catecholate-type siderophores, enterobactin and its glucosylated derivative salmochelin. Although the systems responsible for enterobactin synthesis and acquisition are well characterized, the mechanisms of salmochelin secretion and acquisition, as well as its role in Salmonella virulence, are incompletely understood. Herein we show by liquid chromatography-mass spectrometry analysis of culture supernatants from wild type and isogenic mutant bacterial strains that the Major Facilitator Superfamily pump EntS is the major exporter of enterobactin and the ABC transporter IroC exports both salmochelin and enterobactin. Growth promotion experiments demonstrate that IroC is not required for utilization of Fe-enterobactin or Fe-salmochelin, as had been previously suggested, but the ABC transporter protein FepD is required for utilization of both siderophores. Salmonella mutants deficient in salmochelin synthesis or secretion exhibit reduced virulence during systemic infection of mice.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“The activation and expression of such microbial iron acquisition systems is linked to their pathogenicity and proliferation (Rabsch et al., 1999; Schrettl et al., 2004; Crouch et al., 2008; Andrews-Polymenis et al., 2010; Cassat and Skaar, 2013).”
From Iron at the interface of immunity and infection (2014) · cites this paper as Crouch et al., 2008
In the citing paper
“we infected macrophages with a triple sit feo entC mutant strain of S.Tm defective for the three main iron acquisition pathways (Crouch et al, 2008).”
From Iron Regulatory Proteins Mediate Host Resistance to Salmonella Infection (2015) · cites this paper as Crouch et al, 2008
In the citing paper
“Although, the differences in bacterial counts between ctrl.sh and hmox.sh macrophages were less prominent than during infection with wt Salmonella, intramacrophage numbers of mutant Salmonella were still significantly lower upon hmox silencing than in wt macrophages.”
From Heme oxygenase 1 controls early innate immune response of macrophages to Salmonella Typhimurium infection: Heme oxygenase 1 expression affects Salmonella infection (2016) · cites this paper as Crouch et al., 2008
In the citing paper
“The mutant strain, deficient in enterobactin synthesis, SitABCD- and Feo-mediated iron uptake (ΔentCΔsitΔfeo) was constructed and grown as previously described (Crouch et al., 2008).”
From Heme oxygenase 1 controls early innate immune response of macrophages to Salmonella Typhimurium infection: Heme oxygenase 1 expression affects Salmonella infection (2016) · cites this paper as Crouch et al., 2008
Citations
Cites
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko, K., & Wanner, B. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.120163297 · Cited by 15,902
Guzman, L., Belin, D., Carson, M. J., & Beckwith, J. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4121-4130.1995 · Cited by 4,942
Cherepanov, P., & Wackernagel, W. (1995) · Gene · doi:10.1016/0378-1119(95)00193-a · Cited by 1,952
Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron
Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., & Aderem, A. (2004) · Nature · doi:10.1038/nature03104 · Cited by 1,877
Hentze, M. W., Muckenthaler, M. U., & Andrews, N. C. (2004) · Cell · doi:10.1016/s0092-8674(04)00343-5 · Cited by 1,736
Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg
Vidal, S. M., Malo, D., Vogan, K., Skamene, E., & Gros, P. (1993) · Cell · doi:10.1016/0092-8674(93)90135-d · Cited by 1,104
P-glycoprotein: from genomics to mechanism
Ambudkar, S. V., Kimchi‐Sarfaty, C., Sauna, Z. E., & Gottesman, M. M. (2003) · Oncogene · doi:10.1038/sj.onc.1206948 · Cited by 1,092
Schaible, U. E., & Kaufmann, S. H. E. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro1046 · Cited by 945
Characterization of the ferrous iron uptake system of Escherichia coli
Kammler, M., Schön, C., & Hantke, K. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.19.6212-6219.1993 · Cited by 460
Ochsner, U. A., Wilderman, P. J., Vasil, A. I., & Vasil, M. L. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03084.x · Cited by 406
(2004) · ASM Press eBooks · doi:10.1128/9781555816544 · Cited by 369
Hantke, K., Nicholson, G., Rabsch, W., & Winkelmann, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737682100 · Cited by 359
Andrews, S. C. (1998) · Advances in Microbial Physiology · doi:10.1016/s0065-2911(08)60134-4 · Cited by 353
The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2
Fischbach, M. A., Lin, H., Zhou, L., Yu, Y., Abergel, R. J., Liu, D. R., Raymond, K. N., Wanner, B. L., Strong, R. K., Walsh, C. T., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604636103 · Cited by 319
Forbes, J. R., & Gros, P. (2003) · Blood · doi:10.1182/blood-2003-02-0425 · Cited by 288
The structure of salmochelins: C-glucosylated enterobactins of Salmonella enterica §
Bister, B., Bischoff, D., NICHOLSON, G. J., Valdebenito, M., Schneider, K., Winkelmann, G., Hantke, K., & Süßmuth, R. D. (2004) · BioMetals · doi:10.1023/b:biom.0000029432.69418.6a · Cited by 188
Zhou, D., Hardt, W.-D., & Galán, J. E. (1999) · Infection and Immunity · doi:10.1128/iai.67.4.1974-1981.1999 · Cited by 182
Furrer, J. L., Sanders, D. N., Hook-Barnard, I. G., & McIntosh, M. A. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02885.x · Cited by 180
TolC Is Involved in Enterobactin Efflux across the Outer Membrane of Escherichia coli
Bleuel, C., Große, C., Taudte, N., Scherer, J., Wesenberg, D., Krauss, G.-J., Nies, D. H., & Grass, G. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.19.6701-6707.2005 · Cited by 180
Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse
Tsolis, R. M., Bäumler, A. J., Heffron, F., & Stojiljkovic, I. (1996) · Infection and Immunity · doi:10.1128/iai.64.11.4549-4556.1996 · Cited by 174
In vitro characterization of IroB, a pathogen-associated C -glycosyltransferase
Fischbach, M. A., Lin, H., Liu, D. R., & Walsh, C. T. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408463102 · Cited by 169
IroN, a Novel Outer Membrane Siderophore Receptor Characteristic of Salmonella enterica
Bäumler, A. J., Norris, T. L., Lasco, T., Voigt, W., Reissbrodt, R., Rabsch, W., & Heffron, F. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.6.1446-1453.1998 · Cited by 147
Essential PchG-Dependent Reduction in Pyochelin Biosynthesis of Pseudomonas aeruginosa
Reimmann, C., Patel, H. M., Serino, L., Barone, M., Walsh, C. T., & Haas, D. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.3.813-820.2001 · Cited by 145
Mechanisms of Cellular Iron Acquisition
Kaplan, J. (2002) · Cell · doi:10.1016/s0092-8674(02)01164-9 · Cited by 128
Enterochelin (enterobactin): virulence factor for Salmonella typhimurium
Yancey, R. J., Breeding, S. A., & Lankford, C. E. (1979) · Infection and Immunity · doi:10.1128/iai.24.1.174-180.1979 · Cited by 127
Zaharik, M. L., Cullen, V. L., Fung, A. M., Libby, S. J., Choy, S. L. K., Coburn, B. A., Kehres, D. G., Maguire, M. E., Fang, F. C., & Finlay, B. B. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5522-5525.2004 · Cited by 119
Self-citationFunctions of the siderophore esterases IroD and IroE in iron-salmochelin utilization
Zhu, M., Valdebenito, M., Winkelmann, G., & Hantke, K. (2005) · Microbiology · doi:10.1099/mic.0.27888-0 · Cited by 111
Ferrioxamine-Mediated Iron(III) Utilization by Salmonella enterica
Kingsley, R. A., Reissbrodt, R., Rabsch, W., Ketley, J. M., Tsolis, R. M., Everest, P. H., Gordon Dougan, B., Bäumler, A. J., Roberts, M., & WILLIAMS, P. H. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.4.1610-1618.1999 · Cited by 105
Iron transport by Nramp2/DMT1: pH regulation of transport by 2 histidines in transmembrane domain 6
Lam-Yuk-Tseung, S., Govoni, G. R., Forbes, J., & Gros, P. (2003) · Blood · doi:10.1182/blood-2002-07-2108 · Cited by 104
The effects of mutations in the ant promoter of phage P22 depend on context.
Graña, D., Gardella, T. J., & Susskind, M. M. (1988) · Genetics · doi:10.1093/genetics/120.2.319 · Cited by 99
Benjamin, W. H., Turnbough, C. L., Posey, B. S., & Briles, D. E. (1985) · Infection and Immunity · doi:10.1128/iai.50.2.392-397.1985 · Cited by 90
Binding of Ferric Enterobactin by theEscherichia coliPeriplasmic Protein FepB
Sprencel, C., Cao, Z., Qi, Z., Scott, D. C., Montague, M. A., Ivanoff, N., Xu, J., Raymond, K., Newton, S. M. C., & Klebba, P. E. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.19.5359-5364.2000 · Cited by 82
Rabsch, W., Methner, U., Voigt, W., Tschäpe, H., Reissbrodt, R., & Williams, P. H. (2003) · Infection and Immunity · doi:10.1128/iai.71.12.6953-6961.2003 · Cited by 81
Williams, P. H., Rabsch, W., Methner, U., Voigt, W., Tschäpe, H., & Reissbrodt, R. (2005) · Vaccine · doi:10.1016/j.vaccine.2005.07.020 · Cited by 78
Zhu, W., Arceneaux, J. E. L., Beggs, M. L., Byers, B. R., Eisenach, K. D., & Lundrigan, M. D. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00961.x · Cited by 70
Abergel, R. J., Moore, E. G., Strong, R. K., & Raymond, K. N. (2006) · Journal of the American Chemical Society · doi:10.1021/ja062476+ · Cited by 66
Molecular and clinical aspects of iron homeostasis: from anemia to hemochromatosis
Nairz, M., & Weiß, G. (2006) · Wiener klinische Wochenschrift · doi:10.1007/s00508-006-0653-7 · Cited by 54
Enzymatic Tailoring of Enterobactin Alters Membrane Partitioning and Iron Acquisition
Luo, M., Lin, H., Fischbach, M. A., Liu, D. R., Walsh, C. T., & Groves, J. T. (2006) · ACS Chemical Biology · doi:10.1021/cb0500034 · Cited by 52
Brickman, T. J., & Armstrong, S. K. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.11.3650-3661.2005 · Cited by 48
Page, W. J., Kwon, E. N., Cornish, A. S., & Tindale, A. E. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00753-5 · Cited by 35
Iron-regulated excretion of alpha-keto acids by Salmonella typhimurium
Reissbrodt, R., Kingsley, R. A., Rabsch, W., Beer, W., Roberts, M., & WILLIAMS, P. H. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.14.4538-4544.1997 · Cited by 34
Involvement of the Vibrio parahaemolyticus pvsC gene in export of the siderophore vibrioferrin.
Tanabe, T., Nakao, H., Kuroda, T., Tsuchiya, T., & Yamamoto, S. (2006) · PubMed · Cited by 23
TonB-dependent iron supply inSalmonellaby α-ketoacids and α-hydroxyacids
Kingsley, R. A., Rabsch, W., Roberts, M., Reissbrodt, R., & WILLIAMS, P. H. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08316.x · Cited by 23
Pathogenic Escherichia coli, Shigella , and Salmonella
Payne, S. M., & Mey, A. R. (2014) · ASM Press eBooks · doi:10.1128/9781555816544.ch14 · Cited by 16
A new hydroxamate siderophore for iron supply of Salmonella.
Rabsch, W., Paul, P., & Reissbrodt, R. (1987) · PubMed · Cited by 15
Scheiber‐Mojdehkar, B., & Goldenberg, H. (1996) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1996.0064 · Cited by 14
Research works printed but not linked: 1
- 10.1021/ja062476 · DOI
Cited by
Sorted by citations
Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems
Davidson, A. L., Dassa, E., Orelle, C., & Chen, J. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00031-07 · Cited by 1,477
Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron
Deriu, E., Liu, J. Z., Pezeshki, M., Edwards, R. A., Ochoa, R. J., Contreras, H., Libby, S. J., Fang, F. C., & Raffatellu, M. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.06.007 · Cited by 550
Self-citationRaffatellu, M., George, M. D., Akiyama, Y., Hornsby, M. J., Nuccio, S.-P., Paixao, T. A., Butler, B. P., Chu, H., Santos, R. L., Berger, T., et al. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.03.011 · Cited by 525
Immunometabolism at the interface between macrophages and pathogens
Russell, D. G., Huang, L., & VanderVen, B. C. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0124-9 · Cited by 470
Microbial siderophores: a mini review
Saha, R., Saha, N., Donofrio, R. S., & Bestervelt, L. L. (2012) · Journal of Basic Microbiology · doi:10.1002/jobm.201100552 · Cited by 470
Metadata
- Authors
- Crouch, M. V., Castor, M., Karlinsey, J. E., Kalhorn, T., & Fang, F. C.
- Affiliations
- University of Washington (US)
- Corresponding author
- Fang, Ferric C.
- Venue
- Molecular Microbiology
- Publisher
- Wiley
- Published
- 2008-01-14
- Volume
- 67
- Issue
- 5
- Pages
- 971-983
- ISSN
- 0950-382X (ISSN-L)
- 1365-2958
- OpenAlex
- W2087509245
- Cited by
- 187
- References
- 46
- Citations by year
- 2026: 8 · 2025: 4 · 2024: 6 · 2023: 8 · 2022: 13 · 2021: 10 · 2020: 14 · 2019: 10 · 2018: 6 · 2017: 9 · 2016: 14 · 2015: 12 · 2014: 14 · 2013: 12 · 2012: 11
- FWCI
- 6.33
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI54052, AI 39557, R01AI050660, AI50660, F32AI054052)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Keywords
- salmochelin, enterobactin, siderophore biosynthesis, iron acquisition, iron starvation, Salmonella typhimurium, bacterial virulence, catecholate siderophores, systemic infection
- MeSH terms
- Animals, Bacterial Proteins, Biological Transport, Chromatography, Liquid, Enterobactin, Iron, Membrane Proteins, Salmonella Infections, Animal, Salmonella typhimurium, Mass Spectrometry, Virulence, Siderophores, Sequence Deletion, ATP-Binding Cassette Transporters, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
