The Zur of Xanthomonas campestris functions as a repressor and an activator of putative zinc homeostasis genes via recognizing two distinct sequences within its target promoters

Huang, Dongliang; Tang, Dongjie; Liao, Qing; Li, Heng-Cong; Chen, Qi; He, Yanan; Feng, Jia‐Xun; Jiang, Bo-Le; Lu, Guang‐Tao; Chen, Baoshan

doi:10.1093/nar/gkn328

Cited by 61 publications

(58 citation statements)

References 44 publications

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“…This can be excluded in this study, as we identified Zur boxes in the upstream regions of both Zur-activated genes. Only in one other study, of the phytopathogen Xanthomonas campestris, did Zur act as a direct activator of one gene (22).…”

Section: Discussionmentioning

confidence: 96%

The Zinc-Responsive Regulon of Neisseria meningitidis Comprises 17 Genes under Control of a Zur Element

et al. 2012

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Zinc is a bivalent cation essential for bacterial growth and metabolism. The human pathogenNeisseria meningitidisexpresses a homologue of the Zinc uptake regulator Zur, which has been postulated to repress the putative zinc uptake protein ZnuD. In this study, we elucidated the transcriptome of meningococci in response to zinc by microarrays and quantitative real-time PCR (qRT-PCR). We identified 15 genes that were repressed and two genes that were activated upon zinc addition. All transcription units (genes and operons) harbored a putative Zur binding motif in their promoter regions. A meningococcal Zur binding consensus motif (Zur box) was deducedin silico, which harbors a conserved central palindrome consisting of hexameric inverted repeats separated by three nucleotides (TGTTATDNHATAACA).In vitrobinding of recombinant meningococcal Zur to this Zur box was shown for the first time using electrophoretic mobility shift assays. Zur binding to DNA depended specifically on the presence of zinc and was sensitive to mutations in the palindromic sequence. The Zur regulon among genes of unknown function comprised genes involved in zinc uptake, tRNA modification, and ribosomal assembly. In summary, this is the first study of the transcriptional response to zinc in meningococci.

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Section: Discussionmentioning

confidence: 96%

The Zinc-Responsive Regulon of Neisseria meningitidis Comprises 17 Genes under Control of a Zur Element

et al. 2012

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“…Coelibactin, a putative zincophore, has been recently reported to be regulated by Zur in Streptomyces coelicolor (13,14). In addition, Zur can also act as a direct activator to induce a zinc-export system in Xanthomonas campestris (15).…”

mentioning

confidence: 99%

Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur

Shin

Jung

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

110

189

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Zinc is one of the essential transition metals in cells. Excess or lack of zinc is detrimental, and cells exploit highly sensitive zinc-binding regulators to achieve homeostasis. In this article, we present a crystal structure of active Zur from Streptomyces coelicolor with three zinc-binding sites (C-, M-, and D-sites). Mutations of the three sites differentially affected sporulation and transcription of target genes, such that C- and M-site mutations inhibited sporulation and derepressed all target genes examined, whereas D-site mutations did not affect sporulation and derepressed only a sensitive gene. Biochemical and spectroscopic analyses of representative metal site mutants revealed that the C-site serves a structural role, whereas the M- and D-sites regulate DNA-binding activity as an on-off switch and a fine-tuner, respectively. Consistent with differential effect of mutations on target genes, zinc chelation by TPEN derepressed some genes ( znuA, rpmF2 ) more sensitively than others ( rpmG2 , SCO7682) in vivo. Similar pattern of TPEN-sensitivity was observed for Zur-DNA complexes formed on different promoters in vitro. The sensitive promoters bound Zur with lower affinity than the less sensitive ones. EDTA-treated apo-Zur gained its DNA binding activity at different concentrations of added zinc for the two promoter groups, corresponding to free zinc concentrations of 4.5 × 10 −16 M and 7.9 × 10 −16 M for the less sensitive and sensitive promoters, respectively. The graded expression of target genes is a clever outcome of subtly modulating Zur-DNA binding affinities in response to zinc availability. It enables bacteria to detect metal depletion with improved sensitivity and optimize gene-expression pattern.

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“…This was not the case. In X. campestris Zur controls the expression of both zinc uptake and efflux; thus, when Zur is absent, X. campestris not only undergoes unregulated uptake of zinc, but it also fails to activate zinc efflux systems (19). Our data suggest that, unlike X. campestris Zur, C. diphtheriae Zur is not required for the activation of zinc efflux.…”

Section: Discussionmentioning

confidence: 75%

Regulation and Activity of a Zinc Uptake Regulator, Zur, in Corynebacterium diphtheriae

Smith

Bibb²,

Schmitt³

et al. 2009

J Bacteriol

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Regulation of metal ion homeostasis is essential to bacterial cell survival, and in most species it is controlled by metal-dependent transcriptional regulators. In this study, we describe a Corynebacterium diphtheriae ferric uptake regulator-family protein, Zur, that controls expression of genes involved in zinc uptake. By measuring promoter activities and mRNA levels, we demonstrate that Zur represses transcription of three genes (zrg, cmrA, and troA) in zinc-replete conditions. All three of these genes have similarity to genes involved in zinc uptake. Transcription of zrg and cmrA was also shown to be regulated in response to iron and manganese, respectively, by mechanisms that are independent of Zur. We demonstrate that the activity of the zur promoter is slightly decreased under low zinc conditions in a process that is dependent on Zur itself. This regulation of zur transcription is distinctive and has not yet been described for any other zur. An adjacent gene, predicted to encode a metal-dependent transcriptional regulator in the ArsR/SmtB family, is transcribed from a separate promoter whose activity is unaffected by Zur. A C. diphtheriae zur mutant was more sensitive to peroxide stress, which suggests that zur has a role in protecting the bacterium from oxidative damage. Our studies provide the first evidence of a zinc specific transcriptional regulator in C. diphtheriae and give new insights into the intricate regulatory network responsible for regulating metal ion concentrations in this toxigenic human pathogen.

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The Zur of Xanthomonas campestris functions as a repressor and an activator of putative zinc homeostasis genes via recognizing two distinct sequences within its target promoters

Cited by 61 publications

References 44 publications

The Zinc-Responsive Regulon of Neisseria meningitidis Comprises 17 Genes under Control of a Zur Element

The Zinc-Responsive Regulon of Neisseria meningitidis Comprises 17 Genes under Control of a Zur Element

Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur

Regulation and Activity of a Zinc Uptake Regulator, Zur, in Corynebacterium diphtheriae

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