Differential expression of <i>Bordetella pertussis</i> iron transport system genes during infection

Brickman, Timothy J.; Hanawa, Tomoko; Anderson, Mark T.; Suhadolc, Ryan J.; Armstrong, Sandra K.

doi:10.1111/j.1365-2958.2008.06333.x

Cited by 31 publications

(40 citation statements)

References 28 publications

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“…Expression of the Bordetella alcaligin, enterobactin, and heme receptor genes in infected mice and production of those receptors in human hosts indicate a natural state of iron starvation stress in vivo (21). In the current study, B. pertussis genes encoding the anticipated alcaligin biosynthesis and heme uptake functions, the BfeR regulator of the bfeA enterobactin receptor gene, TonB system genes, and genes encoding TonB-dependent receptors of unknown specificity showed increased transcript abundance under iron starvation conditions.…”

Section: Discussionmentioning

confidence: 75%

“…Similar analyses using a B. pertussis heme receptor mutant demonstrated an in vivo growth defect in the late stages of infection, suggesting that persistence in the host depends on heme utilization (24). The BfeA enterobactin receptor was required for growth of B. pertussis in the early stages of mouse infection (21). Recent studies indicated that B. pertussis upregulates expression of the alcaligin, enterobactin, and heme utilization genes in vivo, confirming that the mammalian host is an iron-restricted environment and that the cognate iron sources are likely present in the host during infection (21).…”

mentioning

confidence: 73%

“…Since the use of these structurally diverse siderophores requires the Fbp system, it is likely that the iron is removed from the siderophores after transit to the periplasm. The Bordetella Fbp system may represent a critical nodal point in iron assimilation in these pathogens, providing an activity essential for iron delivery via siderophores including alcaligin and enterobactin, which are known to be important for multiplication in vivo (20,21).…”

Section: Discussionmentioning

confidence: 99%

“…The BfeA enterobactin receptor was required for growth of B. pertussis in the early stages of mouse infection (21). Recent studies indicated that B. pertussis upregulates expression of the alcaligin, enterobactin, and heme utilization genes in vivo, confirming that the mammalian host is an iron-restricted environment and that the cognate iron sources are likely present in the host during infection (21). Expression patterns of these iron systems were correlated with the stage of infection during which the iron systems appear to have their greatest impact on Bordetella in vivo fitness.…”

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confidence: 99%

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Transcriptional Profiling of the Iron Starvation Response in Bordetella pertussis Provides New Insights into Siderophore Utilization and Virulence Gene Expression

et al. 2011

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Serological studies of patients with pertussis and the identification of antigenic Bordetella pertussis proteins support the hypothesis that B. pertussis perceives an iron starvation cue and expresses multiple iron source utilization systems in its natural human host environment. Furthermore, previous studies using a murine respiratory tract infection model showed that several of these B. pertussis iron systems are required for colonization and persistence and are differentially expressed over the course of infection. The present study examined genome-wide changes in B. pertussis gene transcript abundance in response to iron starvation in vitro. In addition to known iron source utilization genes, we identified a previously uncharacterized iron-repressed cytoplasmic membrane transporter system, fbpABC, that is required for the utilization of multiple structurally distinct siderophores including alcaligin, enterobactin, ferrichrome, and desferrioxamine B. Expression of type III secretion system genes was also found to be upregulated during iron starvation in both B. pertussis strain Tohama I and Bordetella bronchiseptica strain RB50. In a survey of type III secretion system protein production by an assortment of B. pertussis laboratory-adapted and low-passage clinical isolate strains, iron limitation increased the production and secretion of the type III secretion system-specific translocation apparatus tip protein Bsp22 in all Bvg-proficient strains. These results indicate that iron starvation in the infected host is an important environmental cue influencing not only Bordetella iron transport gene expression but also the expression of other important virulence-associated genes.

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Section: Discussionmentioning

confidence: 75%

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confidence: 73%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Transcriptional Profiling of the Iron Starvation Response in Bordetella pertussis Provides New Insights into Siderophore Utilization and Virulence Gene Expression

et al. 2011

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“…These do not appear to be redundant, as mutations in either feo or yfe resulted in a significant growth defect (45). Similarly, Bordetella pertussis uses different systems at different times during infection (46). The alcaligin and enterobactin siderophore systems are expressed early in the course of infection, while heme transport is induced late, reflecting the availability of different iron sources during the course of infection.…”

Section: Discussionmentioning

confidence: 99%

Nonredundant Roles of Iron Acquisition Systems in Vibrio cholerae

et al. 2016

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Vibrio cholerae, the causative agent of the severe diarrheal disease cholera, thrives in both marine environments and the human host. To do so, it must encode the tools necessary to acquire essential nutrients, including iron, under these vastly different conditions. A number of V. cholerae iron acquisition systems have been identified; however, the precise role of each system is not fully understood. To test the roles of individual systems, we generated a series of mutants in which only one of the four systems that support iron acquisition on unsupplemented LB agar, Feo, Fbp, Vct, and Vib, remains functional. Analysis of these mutants under different growth conditions showed that these systems are not redundant. The strain carrying only the ferrous iron transporter Feo grew well at acidic, but not alkaline, pH, whereas the ferric iron transporter Fbp promoted better growth at alkaline than at acidic pH. A strain defective in all four systems (null mutant) had a severe growth defect under aerobic conditions but accumulated iron and grew as well as the wild type in the absence of oxygen, suggesting the presence of an additional, unidentified iron transporter in V. cholerae. In support of this, the null mutant was only moderately attenuated in an infant mouse model of infection. While the null mutant used heme as an iron source in vitro, we demonstrate that heme is not available to V. cholerae in the infant mouse intestine. The Gram-negative bacterium Vibrio cholerae has an absolute requirement for iron (1). Despite the prevalence of iron within its environmental niches and human host, most of this iron is not readily available. Iron occurs naturally as oxidized (ferric) or reduced (ferrous) iron (2). Ferric iron(III), found in oxygenated environments at neutral to alkaline pH, has very low water solubility and forms large insoluble complexes. Studies of ocean water have found iron to be the limiting nutrient for microbial growth (3). Soluble, ferrous iron(II) is more prevalent under the anoxic conditions that V. cholerae may encounter while colonizing the human host. However, access to iron in the host is limited due to competition with other microbes on host surfaces, as well as sequestration by high-affinity iron-binding host proteins such as transferrin and lactoferrin (4-7). Despite the challenges of obtaining iron in these various environments, V. cholerae is proficient in growth in both marine and host environments.The V. cholerae genome encodes multiple iron acquisition systems, which each transport a specific form of iron and may thus optimize iron acquisition in the various niches that V. cholerae inhabits (8-12). These include genes for the synthesis (vib) and utilization (viu) of vibriobactin, a siderophore that is secreted into the environment, where it binds ferric iron with extremely high affinity (9,(13)(14)(15). Ferrivibriobactin is bound by the outer membrane receptor ViuA (16,17) and is transported across the outer membrane in a process that requires either of two energy transduction systems, To...

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