Flanking and Internal Regions of Chromosomal Genes Mediating Aerobactin Iron Uptake Systems in Enteroinvasive Escherichia coli and Shigella flexneri

Marolda, Cristina L.; Valvano, Miguel A.; Lawlor, Kathleen M.; Payne, Shelley M.; Crosa, Jorge H.

doi:10.1099/00221287-133-8-2269

Cited by 30 publications

(50 citation statements)

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“…Aerobactin is a secondary hydroxamate, and genes for its synthesis (iucABCD) and receptor (iutA) are located within a single operon (4,22). These genes may be on either the chromosome (22,24) or a plasmid (4,8). The chromosomal genes are located within PAI in S. flexneri and S. boydii (31,42,57).…”

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Genetics and Virulence Association of the Shigella flexneri Sit Iron Transport System

et al. 2009

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The sit-encoded iron transport system is present within pathogenicity islands in all Shigella spp. and some pathogenic Escherichia coli strains. The islands contain numerous insertion elements and sequences with homology to bacteriophage genes. The Shigella flexneri sit genes can be lost as a result of deletion within the island. The formation of deletions was dependent upon RecA and occurred at relatively high frequency. This suggests that the sit region is inherently unstable, yet sit genes are maintained in all of the clinical isolates tested. Characterization of the sitABCD genes in S. flexneri indicates that they encode a ferrous iron transport system, although the genes are induced aerobically. The sit genes provide a competitive advantage to S. flexneri growing within epithelial cells, and a sitA mutant is outcompeted by the wild type in cultured epithelial cells. The Sit system is also required for virulence in a mouse lung model. The sitA mutant was able to infect the mice and induce a protective immune response but was avirulent compared to its wild-type parent strain.

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Genetics and Virulence Association of the Shigella flexneri Sit Iron Transport System

et al. 2009

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“…Since mutations in tolQ, -R, and -A interfere with the IutA-mediated transport of cloacin DF13 into the cell, we assessed the effect of these mutations on ferric aerobactin transport by a cross-feeding bioassay carried out as described elsewhere (18,19). Strains P9OC(pJHCV8), P9OCtolQ (pJHCV8), TPS300(pJHCV8), C600(pJHCV8), and A592 (pJHCV8), grown under iron-limiting conditions, were cross-fed by exogenously added aerobactin, indicating that tolQ, toiR, and tolA mutations do not affect aerobactinmediated iron uptake (data not shown).…”

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“…Purification of plasmid DNA and transformations were carried out as described elsewhere (30). Outer membrane protein preparations and immunoblot experiments were conducted by following reported procedures (19,31,32). Cloacin DF13 was purified by column chromatography with CM-Sephadex as previously described (8,18), and its 50% killing activity was determined on susceptible cells (E. coli P9OC cells carrying pJHCV8) grown in M9 minimal medium containing 0.1% bovine serum albumin (9,15).…”

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Role of tol genes in cloacin DF13 susceptibility of Escherichia coli K-12 strains expressing the cloacin DF13-aerobactin receptor IutA

Thomas

Valvano

1993

J Bacteriol

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IutA is the outer membrane protein receptor for ferric aerobactin and the bacteriocin cloacin DF13. Although the same receptor is shared, ferric aerobactin transport across the outer membrane in Escherichia coli is TonB dependent, whereas cloacin DF13 transport is not. We have recently observed that tolQ is required for cloacin DF13 susceptibility (J. A. Thomas and M. A. Valvano, FEMS Microbiol. Lett. 91:107-112, 1992). In this study, we demonstrate that the genes tolQ, toiR, and tolA, but not tolB, toWC, and ompF, are required for the internalization of cloacin DF13 and they are not involved in the transport of ferric aerobactin.IutA is an iron-regulated outer membrane protein that serves as a receptor for the hydroxamate siderophore ferric aerobactin (6, 16). In addition, IutA binds the bacteriocin cloacin DF13 (16,34) and presumably the bacteriophage B74K (24). Cloacin DF13 is produced by strains of Enterobacter cloacae and secreted as a protein complex comprising a 56-kDa activity protein and a 10-kDa immunity protein (8). Upon interaction with IutA, the immunity protein is released to the medium while cloacin is translocated across the outer membrane (15). Upon entry into the cell cytoplasm, cloacin can block protein synthesis by causing cleavage of the 16S ribosomal RNA (9, 22).Although both ferric aerobactin and cloacin DF13 interact with IutA primarily at the cell surface (34), the translocation of ferric aerobactin across the outer membrane is TonB dependent, whereas that of cloacin DF13 is not (5, 25). TonB, an inner membrane protein with a large periplasmic domain, interacts with various outer membrane receptors and is essential for the transport of ferrisiderophores, certain bacteriophages, the antibiotic albomycin, and group B colicins such as colicins B, G, D, H, and V (see reference 23 for a review). In contrast, group A colicins (colicins A, El, E2, E3, K, L, N, and S4) and filamentous bacteriophages fl, M13, and fd are TonB independent but they require the products of tol genes for translocation across the outer membrane (see reference 35 for a review). The Tol import system consists of various genes such as tolQ, toiR, tolA, tolB, and toiC whose products are located in different cell compartments; i.e., the inner membrane, periplasmic space, and outer membrane (3,26,27,35 Strains and plasmids used are described in Table 1. Purification of plasmid DNA and transformations were carried out as described elsewhere (30). Outer membrane protein preparations and immunoblot experiments were conducted by following reported procedures (19,31,32). Cloacin DF13 was purified by column chromatography with CM-Sephadex as previously described (8, 18), and its 50% killing activity was determined on susceptible cells (E. coli P9OC cells carrying pJHCV8) grown in M9 minimal medium containing 0.1% bovine serum albumin (9, 15). Cloacin sensitivity was evaluated by a plate killing assay in which 0.5 x 108 microorganisms grown overnight in M9 minimal medium were mixed with molten soft agarose containing the iron chela...

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“…The presence of a colicin system within the pathogenicity island (PAI) of Shigella flexneri upstream of the aerobactin genes further supports the hypothesis of a ColV origin for the chromosomal systems (73). On the other hand, the absence of flanking IS1 sequences both on plasmid-and chromosome-encoded aerobactin systems as well as some sequence divergence, might argue against an IS1-mediated mechanism of dissemination and a ColV origin (74,75).…”

Section: Aerobactin Iron Uptake Systemmentioning

confidence: 85%

Plasmid-Encoded Iron Uptake Systems

Lorenzo

Stork

2014

Microbiol Spectr

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Plasmids confer genetic information that benefits the bacterial cells containing them. In pathogenic bacteria, plasmids often harbor virulence determinants that enhance the pathogenicity of the bacterium. The ability to acquire iron in environments where it is limited, for instance the eukaryotic host, is a critical factor for bacterial growth. To acquire iron, bacteria have evolved specific iron uptake mechanisms. These systems are often chromosomally encoded, while those that are plasmid-encoded are rare. Two main plasmid types, ColV and pJM1, have been shown to harbor determinants that increase virulence by providing the cell with essential iron for growth. It is clear that these two plasmid groups evolved independently from each other since they do not share similarities either in the plasmid backbones or in the iron uptake systems they harbor. The siderophores aerobactin and salmochelin that are found on ColV plasmids fall in the hydroxamate and catechol group, respectively, whereas both functional groups are present in the anguibactin siderophore, the only iron uptake system found on pJM1-type plasmids. Besides siderophore-mediated iron uptake, ColV plasmids carry additional genes involved in iron metabolism. These systems include ABC transporters, hemolysins, and a hemoglobin protease. ColV-and pJM1-like plasmids have been shown to confer virulence to their bacterial host, and this trait can be completely ascribed to their encoded iron uptake systems.

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Flanking and Internal Regions of Chromosomal Genes Mediating Aerobactin Iron Uptake Systems in Enteroinvasive Escherichia coli and Shigella flexneri

Cited by 30 publications

References 20 publications

Genetics and Virulence Association of the Shigella flexneri Sit Iron Transport System

Genetics and Virulence Association of the Shigella flexneri Sit Iron Transport System

Role of tol genes in cloacin DF13 susceptibility of Escherichia coli K-12 strains expressing the cloacin DF13-aerobactin receptor IutA

Plasmid-Encoded Iron Uptake Systems

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