Comparison of the Heme Iron Utilization Systems of Pathogenic Vibrios

O'Malley, Shawn M.; Mouton, S. L.; Occhino, D. A.; Deanda, M. T.; Rashidi, Jeremy; Fuson, K. L.; Rashidi, C. E.; Mora, M; Payne, Shelley M.; Henderson, Douglas P.

doi:10.1128/jb.181.11.3594-3598.1999

Cited by 46 publications

(20 citation statements)

References 27 publications

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“…The presence of more than one TonB system is not unique to V. cholerae. Vibrio parahaemolyticus and Vibrio alginolyticus also contain sequences homologous to tonB1 and tonB2 (O'Malley et al, 1999), and a second tonB gene was identified recently in Pseudomonas aeruginosa (Zhao and Poole, 2000) and may be present in pathogenic Neisseriae (Desai et al, 2000). It will be of interest to determine whether the two TonB proteins have specific functions in these species, as they do in V. cholerae.…”

Section: Discussionmentioning

confidence: 99%

The two TonB systems of Vibrio cholerae: redundant and specific functions

Seliger

Mey

Valle

et al. 2001

Molecular Microbiology

137

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SummaryThe two TonB systems in Vibrio cholerae were found to have unique as well as common functions. Both systems can mediate transport of haemin and the siderophores vibriobactin and ferrichrome. However, TonB1 specifically mediates utilization of the siderophore schizokinen, whereas TonB2 is required for utilization of enterobactin by V. cholerae. Although either TonB system was sufficient for the use of haemin as an iron source, in vitro competition between TonB1 and TonB2 system mutants indicates a preferential role for TonB1 in haemin utilization. This was most pronounced in conditions of high osmolarity, in which TonB1 system mutants were unable to grow with haemin as the sole iron source. Sequence analysis predicted that the two TonB proteins differ in both amino acid sequence and protein size. An internal deletion in TonB1 was constructed in order to generate a protein of approximately the same size as TonB2. A strain expressing the TonB1 deletion protein, and no other TonB, used haemin as the iron source in low-osmolarity medium, but could not use haemin in high osmolarity. This is the same phenotype as a strain expressing only TonB2 and suggests that TonB1, but not TonB2, can span the increased periplasmic space in high osmolarity and thus mediate haemin transport. Mouse colonization assays indicated a role for both TonB systems, and mutations in either system resulted in reduced ability to compete with the wild type in vivo.

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Section: Discussionmentioning

confidence: 99%

The two TonB systems of Vibrio cholerae: redundant and specific functions

Seliger

Mey

Valle

et al. 2001

Molecular Microbiology

137

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“…Earlier studies (Seliger et al, 2001) and data presented here show that V. cholerae relies on the TonB1 system for optimal haem transport, as well as for the utilization of haemoglobin as an iron source. V. alginolyticus, which encodes two TonB systems similar to V. cholerae TonB1 and TonB2, is completely dependent upon the expression of its tonB1 system-like genes for haem utilization (O'Malley et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

Haem utilization in Vibrio cholerae involves multiple TonB‐dependent haem receptors

Mey

Payne

2001

Molecular Microbiology

105

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Vibrio cholerae has multiple iron transport systems, one of which involves haem uptake through the outer membrane receptor HutA. A hutA mutant had only a slight defect in growth using haemin as the iron source, and we show here that V. cholerae encodes two additional TonB‐dependent haem receptors, HutR and HasR. HutR has significant homology to HutA as well as to other outer membrane haem receptors. Membrane fractionation confirmed that HutR is present in the outer membrane. The hutR gene was co‐transcribed with the upstream gene ptrB, and expression from the ptrB promoter was negatively regulated by iron. A hutA, hutR mutant was significantly impaired, but not completely defective, in the ability to use haemin as the sole iron source. HasR is most similar to the haemophore‐utilizing haem receptors from Pseudomonas aeruginosa and Serratia marcescens. A mutant defective in all three haem receptors was unable to use haemin as an iron source. HutA and HutR functioned with either V. cholerae TonB1 or TonB2, but haemin transport through either receptor was more efficient in strains carrying the tonB1 system genes. In contrast, haemin uptake through HasR was TonB2 dependent. Efficient utilization of haemoglobin as an iron source required HutA and TonB1. The triple haem receptor mutant exhibited no defect in its ability to compete with its Vib– parental strain in an infant mouse model of infection, indicating that additional iron sources are present in vivo. V. cholerae used haem derived from marine invertebrate haemoglobins, suggesting that haem may be available to V. cholerae growing in the marine environment.

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“…(Fouz et al. , 1996; O'Malley et al. , 1999; Lemos and Osorio, 2007), cannot be disregarded as a useful strategy to get iron from the environment and hence to survive and multiply in a free‐living state or associated with particulate organic matter.…”

Section: Iron Uptake In the Environmentmentioning

confidence: 99%

Anguibactin‐ versus vanchrobactin‐mediated iron uptake in Vibrio anguillarum: evolution and ecology of a fish pathogen

Lemos

Balado

Osorio

2010

Environ Microbiol Rep

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Vibrio anguillarum is a marine bacterium that is present in many marine aquatic environments and that is the main cause of vibriosis in diverse wild and cultured fish species. Two siderophore-mediated iron uptake systems have been described in V. anguillarum. One, mediated by the siderophore anguibactin, is encoded by the pJM1-type plasmids and is restricted to serotype O1 strains. The second one is mediated by the vanchrobactin siderophore and is widespread in many strains belonging to different serotypes. Both siderophores belong to the catecholate group of siderophores, sharing a 2,3-dihydroxybenzoic acid moiety. Vanchrobactin biosynthesis and transport genes are present in all strains examined although the siderophore is not produced in serotype O1 strains harbouring a pJM1-type plasmid. In these strains the insertion of an IS element in the main vanchrobactin biosynthetic gene vabF leads to the fact that only anguibactin is produced. From our current knowledge we can presume that vanchrobactin is the ancestral siderophore in this species and that the anguibactin-mediated system was later acquired during evolution, likely by horizontal transfer. The role of these two different iron uptake mechanisms in the biology, evolution and ecology of V. anguillarum is discussed although they are still far from being completely understood.

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Comparison of the Heme Iron Utilization Systems of Pathogenic Vibrios

Cited by 46 publications

References 27 publications

The two TonB systems of Vibrio cholerae: redundant and specific functions

The two TonB systems of Vibrio cholerae: redundant and specific functions

Haem utilization in Vibrio cholerae involves multiple TonB‐dependent haem receptors

Anguibactin‐ versus vanchrobactin‐mediated iron uptake in Vibrio anguillarum: evolution and ecology of a fish pathogen

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