Characterization of a Vibrio vulnificus LysR homologue, HupR, which regulates expression of the haem uptake outer membrane protein, HupA

Litwin, Christine M.; Quackenbush, John

doi:10.1006/mpat.2001.0472

Cited by 35 publications

(34 citation statements)

References 47 publications

(23 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Finally, a gene (hupR) coding for a member of the LysR family of transcriptional activators, which regulates expression (21). Homologues of this gene are encountered upstream of V. parahaemolyticus hutA (22) and V. cholerae hutA (12).…”

Section: Resultsmentioning

confidence: 99%

Characterization of Heme Uptake Cluster Genes in the Fish PathogenVibrio anguillarum

2004

View full text Add to dashboard Cite

Vibrio anguillarum can utilize hemin and hemoglobin as sole iron sources. In previous work we identified HuvA, the V. anguillarum outer membrane heme receptor by complementation of a heme utilization mutant with a cosmid clone (pML1) isolated from a genomic library of V. anguillarum. In the present study, we describe a gene cluster contained in cosmid pML1, coding for nine potential heme uptake and utilization proteins: HuvA, the heme receptor; HuvZ and HuvX; TonB, ExbB, and ExbD; HuvB, the putative periplasmic binding protein; HuvC, the putative inner membrane permease; and HuvD, the putative ABC transporter ATPase. A V. anguillarum strain with an in-frame chromosomal deletion of the nine-gene cluster was impaired for growth with heme or hemoglobin as the sole iron source. Single-gene in-frame deletions were constructed, demonstrating that each of the huvAZBCD genes are essential for utilization of heme as an iron source in V. anguillarum, whereas huvX is not. When expressed in Escherichia coli hemA (strain EB53), a plasmid carrying the gene for the heme receptor, HuvA, was sufficient to allow the use of heme as the porphyrin source. For utilization of heme as an iron source in E. coli ent (strain 101ESD), the tonB exbBD and huvBCD genes were required in addition to huvA. The V. anguillarum heme uptake cluster shows some differences in gene arrangement when compared to homologous clusters described for other Vibrio species.Iron is an essential element for most bacteria, serving as a cofactor in key metabolic processes such as nucleotide biosynthesis, electron transfer, and energy transduction. Most bacterial pathogens require iron for growth and to establish an infection, and thus they have developed efficient mechanisms to obtain iron from the host (32). The small amounts of extracellular iron are quickly bound by high-affinity carrier proteins such as transferrin in serum and lactoferrin in secretions. Vibrio anguillarum is the etiological agent of a septicemic disease known as vibriosis, which affects a large number of marine fish species. Within the 10 O serogroups described by Sørensen and Larsen (35), only serotypes O1 and O2 and, to a lesser extent, serotype O3 are considered important fish pathogens. Although V. anguillarum is the best known fish pathogen of the genus Vibrio, the nature of its virulence mechanisms is not thoroughly understood. Strains of pathogenic V. anguillarum serotypes can acquire iron by the production and secretion of siderophores (2,4,16,19,38). Heme and some heme-containing proteins, including hemoglobin and hemoglobin-haptoglobin, can also be used as iron sources by a siderophore-independent mechanism (23,24).In this way, many gram-negative pathogens have the ability to obtain iron through utilization of free heme or heme proteins from the host tissues (7, 18), and heme utilization genes have been identified in numerous species, including Yersinia enterocolitica (36, 37), Vibrio cholerae (13,26,29), Escherichia coli O157 (39), Vibrio vulnificus (20), Plesiomonas shigelloides (1...

show abstract

Section: Resultsmentioning

confidence: 99%

Characterization of Heme Uptake Cluster Genes in the Fish PathogenVibrio anguillarum

2004

View full text Add to dashboard Cite

show abstract

“…Various Fur-augmented regulatory systems have been described previously: siderophore-responsive transcription is dependent on AraC-type regulators in both Pseudomonas aeruginosa (14) and Bordetella spp. (2), LysR-type regulators have been implicated in the heme-responsive gene expression of Vibrio vulnificus (20) and Bradyrhizobium japonicum (12), and classical two-component sensor-kinase pairs have been described for Corynebacterium diphtheriae (25) and Pseudomonas aeruginosa (6). Sigma () factors, particularly those denoted as extracytoplasmic function (ECF) factors, also participate in Fur-dependent gene regulation.…”

mentioning

confidence: 99%

Transcriptional Control of the rhuIR-bhuRSTUV Heme Acquisition Locus in Bordetella avium

King

Kirby²,

Connell

2005

Infect Immun

View full text Add to dashboard Cite

Iron (Fe) is an essential nutrient for most bacterial pathogens. In these organisms, a variety of regulatory systems that respond to specific Fe complexes found within their vertebrate hosts have evolved. In Bordetella avium, the heme utilization locus encoded by rhuIR-bhuRSTUV mediates efficient acquisition of Fe from heme and hemoproteins. Control of bhuRSTUV expression is promulgated at two levels. When Fe is abundant, expression is repressed in a Fur-dependent manner which is partially relieved when Fe is limiting. In the presence of heme or hemoproteins, expression of the bhuRSTUV operon is induced via a three-component signal transduction cascade composed of RhuI, RhuR, and BhuR. Herein, we report the identification of two promoters (P rhuI and P bhuR ) that control expression of the rhuIR-bhuRSTUV cluster. Primer extension analysis identified the transcriptional start site of P rhuI within a putative Fur box. Transcriptional initiation of P bhuR mapped within the rhuR-bhuR intergenic region. Maximal transcription from P bhuR required Fe-limiting conditions, the presence of heme (or hemoglobin), and rhuI; however, analysis of transcripts produced from the rhuIR-bhuRSTUV locus revealed a pattern of low-level bhuR transcription in the absence of heme which originated from both P bhuR and P rhuI . Transcription from P rhuI was repressed by Fe in the presence of fur and somewhat enhanced by the addition of hemin to Fe-limited media. The nature of this hemin-associated P rhuI stimulation was rhuI independent and therefore not induced by heme via the BhuR-RhuR-RhuI signal cascade. Fe also repressed transcription from P bhuR in a fur-dependent manner; however, activation from this promoter, in the presence or absence of heme, did not occur without rhuI.

show abstract

“…Other examples of positive regulation are the activation of irgA, encoding a V. cholerae enterobactin receptor, and hupR, encoding the V. vulnificus heme receptor, both of which are divergently transcribed from positive regulators. IrgB activates the transcription of irgA (228,229), and HupR induces hupA (230). Both IrgB and HupR are members of the LysR family of positive transcriptional activators (228,230).…”

Section: Regulation Of Iron Transport Systemsmentioning

confidence: 99%

“…IrgB activates the transcription of irgA (228,229), and HupR induces hupA (230). Both IrgB and HupR are members of the LysR family of positive transcriptional activators (228,230). A number of other Vibrio iron transport genes, including vctA, have known or putative regulators that are divergently transcribed.…”

Section: Regulation Of Iron Transport Systemsmentioning

confidence: 99%

Vibrio Iron Transport: Evolutionary Adaptation to Life in Multiple Environments

Payne

Mey

Wyckoff

2016

Microbiol Mol Biol Rev

View full text Add to dashboard Cite

SUMMARYIron is an essential element forVibriospp., but the acquisition of iron is complicated by its tendency to form insoluble ferric complexes in nature and its association with high-affinity iron-binding proteins in the host. Vibrios occupy a variety of different niches, and each of these niches presents particular challenges for acquiring sufficient iron.Vibriospecies have evolved a wide array of iron transport systems that allow the bacteria to compete for this essential element in each of its habitats. These systems include the secretion and uptake of high-affinity iron-binding compounds (siderophores) as well as transport systems for iron bound to host complexes. Transporters for ferric and ferrous iron not complexed to siderophores are also common toVibriospecies. Some of the genes encoding these systems show evidence of horizontal transmission, and the ability to acquire and incorporate additional iron transport systems may have allowedVibriospecies to more rapidly adapt to new environmental niches. While too little iron prevents growth of the bacteria, too much can be lethal. The appropriate balance is maintained in vibrios through complex regulatory networks involving transcriptional repressors and activators and small RNAs (sRNAs) that act posttranscriptionally. Examination of the number and variety of iron transport systems found inVibriospp. offers insights into how this group of bacteria has adapted to such a wide range of habitats.

show abstract

Characterization of a Vibrio vulnificus LysR homologue, HupR, which regulates expression of the haem uptake outer membrane protein, HupA

Cited by 35 publications

References 47 publications

Characterization of Heme Uptake Cluster Genes in the Fish PathogenVibrio anguillarum

Characterization of Heme Uptake Cluster Genes in the Fish PathogenVibrio anguillarum

Transcriptional Control of the rhuIR-bhuRSTUV Heme Acquisition Locus in Bordetella avium

Vibrio Iron Transport: Evolutionary Adaptation to Life in Multiple Environments

Contact Info

Product

Resources

About