Campylobacter jejuni ferric–enterobactin receptor CfrA is TonB3 dependent and mediates iron acquisition from structurally different catechol siderophores

Naikare, Hemant; Butcher, James; Flint, Annika; Xu, Jide; Raymond, Kenneth N.; Stintzi, Alain

doi:10.1039/c3mt20254b

Cited by 32 publications

(30 citation statements)

References 42 publications

(128 reference statements)

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“…The present study is focused on the identification of cognate TonB system(s) for the two different FeEnt acquisition pathways in Campylobacter (Zeng et al ., ). We demonstrated that TonB3 plays a dominant role in CfrA‐dependent FeEnt acquisition, which is consistent with the finding from a recent report (Naikare et al ., ). However, in the CfrB‐dependent pathway, TonB2 and TonB3 are interchangeable for efficient FeEnt acquisition.…”

Section: Discussionmentioning

confidence: 97%

Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition inCampylobacter

Zeng

Xu²,

Lin

2013

FEMS Microbiol Lett

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Ferric enterobactin (FeEnt) acquisition plays a critical role in the pathophysiology of Campylobacter, the leading bacterial cause of human gastroenteritis in industrialized countries. In Campylobacter, the surface-exposed receptor, CfrA or CfrB, functions as a “gatekeeper” for initial binding of FeEnt. Subsequent transport across the outer membrane is energized by TonB-ExbB-ExbD energy transduction systems. Although there are up to three TonB-ExbB-ExbD systems in Campylobacter, the cognate components of TonB-ExbB-ExbD for FeEnt acquisition are still largely unknown. In this study, we addressed this issue using complementary molecular approaches including: comparative genomic analysis, random transposon mutagenesis, and site-directed mutagenesis in two representative C. jejuni strains, NCTC 11168 and 81-176. We demonstrated that CfrB could interact with either TonB2 or TonB3 for efficient Ent-mediated iron acquisition. However, TonB3 is a dominant player in CfrA-dependent pathway. The ExbB2 and ExbD2 components were essential for both CfrA- and CfrB-dependent FeEnt acquisition. Sequences analysis identified potential TonB boxes in CfrA and CfrB, and the corresponding binding sites in TonB. In conclusion, these findings reveal identities of specific TonB-ExbB-ExbD energy transduction components required for FeEnt acquisition, and provide insights into the complex molecular interactions of FeEnt acquisition systems in Campylobacter.

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Section: Discussionmentioning

confidence: 97%

Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition inCampylobacter

Zeng

Xu²,

Lin

2013

FEMS Microbiol Lett

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“…It is likely to be transported by one or more of these catechol siderophore receptors, but this has not been determined. Recent work in Campylobacter jejuni shows that the ability of a single outer membrane receptor to transport multiple, related ligands is not limited to V. cholerae receptors (40), and this may represent an underappreciated aspect of siderophore biology.…”

Section: Figmentioning

confidence: 99%

Catechol Siderophore Transport by Vibrio cholerae

et al. 2015

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Siderophores, small iron-binding molecules secreted by many microbial species, capture environmental iron for transport back into the cell. Vibrio cholerae synthesizes and uses the catechol siderophore vibriobactin and also uses siderophores secreted by other species, including enterobactin produced by Escherichia coli. E. coli secretes both canonical cyclic enterobactin and linear enterobactin derivatives likely derived from its cleavage by the enterobactin esterase Fes. We show here that V. cholerae does not use cyclic enterobactin but instead uses its linear derivatives. V. cholerae lacked both a receptor for efficient transport of cyclic enterobactin and enterobactin esterase to promote removal of iron from the ferrisiderophore complex. To further characterize the transport of catechol siderophores, we show that the linear enterobactin derivatives were transported into V. cholerae by either of the catechol siderophore receptors IrgA and VctA, which also transported the synthetic siderophore MECAM [1,3,5-N,N=,N؆-tris-(2,3-dihydroxybenzoyl)-triaminomethylbenzene]. Vibriobactin is transported via the additional catechol siderophore receptor ViuA, while the Vibrio fluvialis siderophore fluvibactin was transported by all three catechol receptors. ViuB, a putative V. cholerae siderophore-interacting protein (SIP), functionally substituted for the E. coli ferric reductase YqjH, which promotes the release of iron from the siderophore in the bacterial cytoplasm. In V. cholerae, ViuB was required for the use of vibriobactin but was not required for the use of MECAM, fluvibactin, ferrichrome, or the linear derivatives of enterobactin. This suggests the presence of another protein in V. cholerae capable of promoting the release of iron from these siderophores. IMPORTANCEVibrio cholerae is a major human pathogen and also serves as a model for the Vibrionaceae, which include other serious human and fish pathogens. The ability of these species to persist and acquire essential nutrients, including iron, in the environment is epidemiologically important but not well understood. In this work, we characterize the ability of V. cholerae to acquire iron by using siderophores produced by other organisms. We resolve confusion in the literature regarding its ability to use the Escherichia coli siderophore enterobactin and identify the receptor and TonB system used for the transport of several siderophores. The use of some siderophores did not require the ferric reductase ViuB, suggesting that an uncharacterized ferric reductase is present in V. cholerae.

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“…It is not surprising that, as a scavenger, C. jejuni can utilize a diverse range of catecholate siderophores for the uptake of Fe(III), including tetradentate siderophores such as azotochelin and the enterobactin-derived bis(2,3-dihydroxybenzoyl-L-Ser) (Fig. 1)17. Indeed, the periplasmic enterobactin esterase Cee has been shown to play an important role in the uptake of Fe(III) in C. jejuni , since it hydrolyzes the enterobactin backbone in the periplasm followed by the import of Fe(III)-enterobactin fragment complexes, including bis(2,3-dihydroxybenzoyl-L-Ser), into the cytoplasm18.…”

mentioning

confidence: 99%

Interactions of the periplasmic binding protein CeuE with Fe(III) n-LICAM4− siderophore analogues of varied linker length

Wilde

Hughes

Blagova

et al. 2017

Sci Rep

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Bacteria use siderophores to mediate the transport of essential Fe(III) into the cell. In Campylobacter jejuni the periplasmic binding protein CeuE, an integral part of the Fe(III) transport system, has adapted to bind tetradentate siderophores using a His and a Tyr side chain to complete the Fe(III) coordination. A series of tetradentate siderophore mimics was synthesized in which the length of the linker between the two iron-binding catecholamide units was increased from four carbon atoms (4-LICAM4−) to five, six and eight (5-, 6-, 8-LICAM4−, respectively). Co-crystal structures with CeuE showed that the inter-planar angles between the iron-binding catecholamide units in the 5-, 6- and 8-LICAM4− structures are very similar (111°, 110° and 110°) and allow for an optimum fit into the binding pocket of CeuE, the inter-planar angle in the structure of 4-LICAM4− is significantly smaller (97°) due to restrictions imposed by the shorter linker. Accordingly, the protein-binding affinity was found to be slightly higher for 5- compared to 4-LICAM4− but decreases for 6- and 8-LICAM4−. The optimum linker length of five matches that present in natural siderophores such as enterobactin and azotochelin. Site-directed mutagenesis was used to investigate the relative importance of the Fe(III)-coordinating residues H227 and Y288.

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Campylobacter jejuni ferric–enterobactin receptor CfrA is TonB3 dependent and mediates iron acquisition from structurally different catechol siderophores

Cited by 32 publications

References 42 publications

Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition inCampylobacter

Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition inCampylobacter

Catechol Siderophore Transport by Vibrio cholerae

Interactions of the periplasmic binding protein CeuE with Fe(III) n-LICAM4− siderophore analogues of varied linker length

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