Characterization of Vibrio parahaemolyticus genes encoding the systems for utilization of enterobactin as a xenosiderophore

Tanabe, T.; Funahashi, Tatsuya; Shiuchi, Keiichi; Okajima, Noriyuki; Nakao, Hiroshi; Miyamoto, Katsushiro; Tsujibo, Hiroshi; Yamamoto, Satoshi

doi:10.1099/mic.0.059568-0

Cited by 19 publications

(29 citation statements)

References 53 publications

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“…Several members of the Vibrionaceae have been shown to transport enterobactin, including Vibrio parahaemolyticus (41), Aeromonas hydrophila (42), and Vibrio anguillarum (43), and homologues of IrgA and/or VctA are found in the sequenced genomes of a number of members of the Vibrionaceae (Table 5 shows selected homologues). V. fluvialis, Vibrio vulnificus, Vibrio alginolyticus, and V. parahaemolyticus have been reported to use vibriobactin (24), and the vulnibactin receptors of V. vulnificus (44) and V. fluvialis have significant sequence similarity with ViuA (Table 5).…”

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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Section: Figmentioning

confidence: 99%

Catechol Siderophore Transport by Vibrio cholerae

et al. 2015

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“…Primer extension of ryhB was carried out using the VpryhB-PE primer (see Table S1 in the supplemental material), 5= labeled with Texas Red, and an SQ5500 DNA sequencer (Hitachi, Tokyo, Japan) as previously described (49). Construction of deletion and complementary replacement mutants.…”

Section: Rna Was Extracted With the Rneasy Protect Bacterial Mini Kitmentioning

confidence: 99%

“…parahaemolyticus is a halophilic Gram-negative bacterium that typically inhabits sea and brackish water, and it can cause diarrhea and gastroenteritis upon consumption of seafood contaminated with the bacterium (44,45). It has been previously reported that V. parahaemolyticus is able to utilize some siderophores, including the cognate vibrioferrin (46), exogenous aerobactin (47), ferrichrome (48), and enterobactin (49), to acquire iron under iron-depleted conditions. The Fur-regulated gene cluster involved in the vibrioferrin-mediated iron acquisition system is composed of 2 divergent operons that contain pvsABCDE (pvsABDE, vibrioferrin biosynthesis genes; pvsC, vibrioferrin exporter gene) (Fig.…”

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confidence: 99%

The Vibrio parahaemolyticus Small RNA RyhB Promotes Production of the Siderophore Vibrioferrin by Stabilizing the Polycistronic mRNA

et al. 2013

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In this study, we identified the Fur-regulated small RNA RyhB and the RNA chaperone Hfq protein as additional regulatory proteins of vibrioferrin biosynthesis. We found that vibrioferrin production was greatly impaired in both the ryhB and hfq deletion mutants, and a TargetRNA search (http://snowwhite.wellesley.edu/targetRNA/index2.html) revealed that the 5=-untranslated region of pvsOp mRNA (pvsOp 5=-UTR) contains a potential base-pairing region required for the formation of the RyhB-pvsOp 5=-UTR duplex. An electrophoresis mobility shift assay indicated that RyhB can directly bind to the pvsOp 5=-UTR with the aid of Hfq. Rifampin chase experiments indicated that the half-life of pvsOp mRNA in the ryhB and hfq mutants was approximately 3-fold shorter than that in the parental strain, suggesting that both RyhB and Hfq are engaged in the stabilization of pvsOp mRNA. Chrome azurol S assays followed by electrophoresis mobility shift assays and rifampin chase experiments carried out for mutant strains indicated that base pairing between RyhB and the pvsOp 5=-UTR results in an increase in the stability of pvsOp mRNA, thereby leading to the promotion of vibrioferrin production. It is unprecedented that RyhB confers increased stability on a polycistronic mRNA involved in siderophore biosynthesis as a direct target.

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“…We previously reported that V. parahaemolyticus can utilize ferric Ent as an iron source via the VctA and IrgA receptors [27]. Although the VPD54 mutant with deletion of vctA and irgA that was generated from the VPD5 vibrioferrin-deficient mutant failed to grow in LB-Tris/+EDDA medium at pH 7.0 and 8.0, it showed normal growth when Ent was added to LB-Tris/+EDDA medium (LB-Tris/+EDDA/+Ent) at pH 8.0, but not at pH 7.0 (Figure 1).…”

Section: Resultsmentioning

confidence: 99%

“…Under iron-limiting conditions, this bacterium secretes its own siderophore, vibrioferrin [21], which is biosynthesized by four enzymes encoded by pvsABDE [22], and transports extracellular iron as ferric vibrioferrin back to the cell via two OMRs specific to ferric vibrioferrin and the ABC transporter complex, which are encoded by pvuA1-pvuA2 and pvuBCDE , respectively [22]–[24]. In addition to producing vibrioferrin, V. parahaemolyticus can utilize aerobactin [25], ferrichrome [26], and Ent [27] as xenosiderophores by expressing their cognate OMRs.…”

Section: Introductionmentioning

confidence: 99%

Regulation of the Expression of the Vibrio parahaemolyticus peuA Gene Encoding an Alternative Ferric Enterobactin Receptor

et al. 2014

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A pvsB-vctA-irgA triple deletion mutant of Vibrio parahaemolyticus can utilize enterobactin under iron-limiting conditions by inducing a previously undescribed receptor, PeuA (VPA0150), in response to extracellular alkaline pH and enterobactin. In silico analyses revealed the existence of a two-component regulatory system operon, peuRS, immediately upstream of peuA, which constitutes an operon with the TonB2 system genes. Both the peuRS and peuA-tonB2 operons were found to be upregulated under iron-limiting conditions in a ferric uptake regulator (Fur)-dependent manner. The involvement of peuA and peuRS in enterobactin utilization was analyzed by complementation experiments using deletion mutants. Primer extension analysis indicated that, under iron-limiting conditions, the transcription of peuA was initiated from the +1 site at pH 7.0 and from both the +1 and +39 sites at pH 8.0 in the presence of enterobactin. The +39 transcript was absent from the peuRS deletion mutant. Secondary structure prediction of their 5′-untranslated regions suggested that translation initiation is blocked in the +1 transcript, but not in the +39 transcript. Consistent with this, in vitro translation analysis demonstrated that production of PeuA was determined only by the +39 transcript. These studies establish a novel gene regulation mechanism in which the two-component regulatory system PeuRS enhances expression of the alternative +39 transcript that possesses non-inhibitory structure, allowing the peuA expression to be regulated at the translation stage.

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Characterization of Vibrio parahaemolyticus genes encoding the systems for utilization of enterobactin as a xenosiderophore

Cited by 19 publications

References 53 publications

Catechol Siderophore Transport by Vibrio cholerae

Catechol Siderophore Transport by Vibrio cholerae

The Vibrio parahaemolyticus Small RNA RyhB Promotes Production of the Siderophore Vibrioferrin by Stabilizing the Polycistronic mRNA

Regulation of the Expression of the Vibrio parahaemolyticus peuA Gene Encoding an Alternative Ferric Enterobactin Receptor

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