Iron stress increases<i>Bordetella pertussis</i>mucin-binding capacity and attachment to respiratory epithelial cells

Vidakovics, María Laura Anabella Pérez; Lamberti, Yanina Andrea; Serra, Diego O.; Berbers, Guy A. M.; Pol, W. Ludo van der; Rodrı́guez, Marı́a Eugenia

doi:10.1111/j.1574-695x.2007.00320.x

Cited by 11 publications

(12 citation statements)

References 29 publications

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“…Iron-starved B. pertussis was shown to adhere more effectively to A549 human alveolar epithelial cells compared with iron-replete bacteria (89). A B. pertussis tonB mutant was attenuated in a mouse model of infection (70), and a B. bronchiseptica alcaligin siderophore biosynthesis mutant showed decreased virulence in neonatal swine (73).…”

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confidence: 99%

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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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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“…The Iha receptor has been implicated in utilization of catecholate as a nutrient and in adherence of the bacterium to epithelial cells (41). B. pertussis cultured under Fe-stressed conditions exhibited enhanced attachment to epithelial cells (70). The Fe-dependent adhesin which mediates this attachment has not been firmly identified.…”

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confidence: 99%

“…1A). Putative Ϫ35 (5Ј-TTGATA-3Ј) and Ϫ10 (5Ј-TTAATA-3Ј) hexameric regions of P ecfIR exhibited similarities to promoters usually regulated by 70 ( Fig. 1B) (36).…”

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confidence: 94%

“…The 534-bp ORF located most distal to bfrH, designated ecfI, 70 family of sigma factors which regulates binding of the sigma factor to promoters only when the sigma factor is associated with RNA polymerase, is shortened or missing in ECF sigma factors (43). Amino acid analysis indicated that regions 2 and 4 were significantly conserved in EcfI.…”

Section: Identification Of Bfrhmentioning

confidence: 99%

“…(B) Sequences at P ecfIR . This promoter contains regions homologous to 70 -type promoters. Putative Ϫ10 and Ϫ35 regions of P ecfIR are boxed.…”

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confidence: 99%

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Expression of BfrH, a Putative Siderophore Receptor of Bordetella bronchiseptica , Is Regulated by Iron, Fur1, and the Extracellular Function Sigma Factor EcfI

2010

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Iron (Fe) in soluble elemental form is found in the tissues and fluids of animals at concentrations insufficient for sustaining growth of bacteria. Consequently, to promote colonization and persistence, pathogenic bacteria evolved a myriad of scavenging mechanisms to acquire Fe from the host. Bordetella bronchiseptica, the etiologic agent of upper respiratory infections in a wide range of mammalian hosts, expresses a number of proteins for acquisition of Fe. Using proteomic and genomic approaches, three Fe-regulated genes were identified in the bordetellae: bfrH, a gene encoding a putative siderophore receptor; ecfI, a gene encoding a putative extracellular function (ECF) sigma factor; and ecfR, a gene encoding a putative EcfI modulator. All three genes are highly conserved in B. pertussis, B. parapertussis, and B. avium. Genetic analysis revealed that transcription of bfrH was coregulated by ecfI, ecfR, and fur1, one of two fur homologues carried by B. bronchiseptica. Overexpression of ecfI decoupled bfrH from Fe-dependent regulation. In contrast, expression of bfrH was significantly reduced in an ecfI deletion mutant. Deletion of ecfR, however, was correlated with a significant increase in expression of bfrH, due in part to a cis-acting nucleotide sequence within ecfR which likely reduces the frequency of readthrough transcription of bfrH from the Fe-dependent ecfIR promoter. Using a murine competition infection model, bfrH was shown to be required for optimal virulence of B. bronchiseptica. These experiments revealed ecfIR-bfrH as a locus encoding a new member of the growing family of Fe and ECF sigma factor-modulated regulons in the bordetellae.

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Shotgun proteome analysis of Bordetella pertussis reveals a distinct influence of iron availability on the bacterial metabolism, virulence, and defense response

et al. 2015

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One of the mechanisms involved in host immunity is the limitation of iron accessibility to pathogens, which in turn provokes the corresponding physiological adaptation of pathogens. This study reports a gel-free nanoLC-MS/MS-based comparative proteome analysis of Bordetella pertussis grown under iron-excess and iron-depleted conditions. Out of the 926 proteins covered 98 displayed a shift in their abundance in response to low iron availability. Forty-seven of them were found to be increased in level while 58 were found with decreased protein levels under iron starvation. In addition to proteins previously reported to be influenced by iron in B. pertussis, we observed changes in metabolic proteins involved in fatty acid utilization and poly-hydroxybutyrate production. Additionally, many bacterial virulence factors regulated by the BvgAS two-component system were found at decreased levels in response to iron limitation. These results, together with the increased production of proteins potentially involved in oxidative stress resistance, seem to indicate that iron starvation provokes changes in B. pertussis phenotype that might shape host-pathogen interaction.

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Iron stress increasesBordetella pertussismucin-binding capacity and attachment to respiratory epithelial cells

Cited by 11 publications

References 29 publications

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

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

Expression of BfrH, a Putative Siderophore Receptor of Bordetella bronchiseptica , Is Regulated by Iron, Fur1, and the Extracellular Function Sigma Factor EcfI

Shotgun proteome analysis of Bordetella pertussis reveals a distinct influence of iron availability on the bacterial metabolism, virulence, and defense response

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