Identifying the region responsible for Brucella abortus MucR higher-order oligomer formation and examining its role in gene regulation

Pirone, Luciano; Pitzer, Joshua E.; D’Abrosca, Gianluca; Fattorusso, Roberto; Malgieri, Gaetano; Pedone, Emilia; Pedone, Paolo V.; Roop, R. Martin; Baglivo, Ilaria

doi:10.1038/s41598-018-35432-1

Cited by 15 publications

(30 citation statements)

References 75 publications

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“…This is in agreement with what we observed with the other proteins of the Ros/MucR family and it is likely due to the aggregation propensity of these proteins being able to form higher-order oligomers [12,37]. We previously proposed that MucR binds to DNA via low specificity interactions with AT-rich regions in a manner reminiscent of H-NS [13,14]. H-NS demonstrates a broad range of affinities for AT-rich regions, and the capacity of this protein to function as a transcriptional regulator is strongly influenced by its affinity for specific DNA-target sites [38].…”

Section: Mucr Binds the Promoters Of Babr And Virb Genessupporting

confidence: 92%

“…In C. crescentus, the protein MucR is also involved in the cell cycle progression [42] and notably the Brucella cell cycle has been linked to this bacterium's pathogenic potential [43]. Recently, we have demonstrated that MucR can form higher-order oligomers and binds AT-rich sequences containing T-A steps [12][13][14]. These findings led us to compare the role of MucR in the α-proteobacteria to that of H-NS proteins that regulate the expression of virulence genes in βand γ-proteobacteria.…”

Section: Discussionmentioning

confidence: 99%

“…The gene encoding BabR has been shown to be strongly repressed by MucR in both B. abortus 2308 [4,14] and B. melitensis 16M [33]. The promoter of the B. abortus babR gene has been characterized in detail by Caswell et al [22].…”

Section: Mucr Binds the Promoters Of Babr And Virb Genesmentioning

confidence: 99%

“…The babR20.2M failed to bind MucR (Figure 2c) demonstrating that T-A steps mutated in this oligonucleotide play an important role in the MucR interaction with babR promoter. We have recently reported that MucR could be a histone-like (H-NS) protein able to form higherorder oligomers and recognizing AT-rich sequences containing T-A steps like the H-NS proteins present in βand γ-proteobacteria [13,14,34]. To gain a clearer picture of the individual contributions of specific AT-rich regions within the babR promoter to MucR binding, we designed three 20 bp oligonucleotides, named babR20.1, babR20.2 and babR20.3, whose sequences represent overlapping segments of babR60 (Figures 1 and 2b).…”

Section: Mucr Binds the Promoters Of Babr And Virb Genesmentioning

confidence: 99%

“…Recently, we have demonstrated that the Mls and MucR form higher-order oligomers and interact mostly with the DNA minor groove recognizing AT-rich DNA sequences containing T-A steps. These findings led us to suggest that members of the Ros/MucR family could play the same role in α-proteobacteria in regulating virulence gene expression as the histone-like proteins H-NS in βand γ-proteobacteria [12][13][14]. In fact, H-NS proteins regulate virulence gene expression by binding AT-rich sequences containing T-A steps [15].…”

Section: Introductionmentioning

confidence: 99%

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Different Impacts of MucR Binding to the babR and virB Promoters on Gene Expression in Brucella abortus 2308

Borriello¹,

Russo

Paradiso³

et al. 2020

Biomolecules

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The protein MucR from Brucella abortus has been described as a transcriptional regulator of many virulence genes. It is a member of the Ros/MucR family comprising proteins that control the expression of genes important for the successful interaction of α-proteobacteria with their eukaryotic hosts. Despite clear evidence of the role of MucR in repressing virulence genes, no study has been carried out so far demonstrating the direct interaction of this protein with the promoter of its target gene babR encoding a LuxR-like regulator repressing virB genes. In this study, we show for the first time the ability of MucR to bind the promoter of babR in electrophoretic mobility shift assays demonstrating a direct role of MucR in repressing this gene. Furthermore, we demonstrate that MucR can bind the virB gene promoter. Analyses by RT-qPCR showed no significant differences in the expression level of virB genes in Brucella abortus CC092 lacking MucR compared to the wild-type Brucella abortus strain, indicating that MucR binding to the virB promoter has little impact on virB gene expression in B. abortus 2308. The MucR modality to bind the two promoters analyzed supports our previous hypothesis that this is a histone-like protein never found before in Brucella.

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Section: Mucr Binds the Promoters Of Babr And Virb Genessupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Mucr Binds the Promoters Of Babr And Virb Genesmentioning

confidence: 99%

Section: Mucr Binds the Promoters Of Babr And Virb Genesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Different Impacts of MucR Binding to the babR and virB Promoters on Gene Expression in Brucella abortus 2308

Borriello¹,

Russo

Paradiso³

et al. 2020

Biomolecules

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Ancestral zinc-finger bearing protein MucR in alpha-proteobacteria: A novel xenogeneic silencer?

Jiao

Tian

2020

Computational and Structural Biotechnology Journal

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The MucR/Ros family protein is conserved in alpha-proteobacteria and characterized by its zinc-finger motif that has been proposed as the ancestral domain from which the eukaryotic C2H2 zinc-finger structure evolved. In the past decades, accumulated evidences have revealed MucR as a pleiotropic transcriptional regulator that integrating multiple functions such as virulence, symbiosis, cell cycle and various physiological processes. Scattered reports indicate that MucR mainly acts as a repressor, through oligomerization and binding to multiple sites of AT-rich target promoters. The N-terminal region and zinc-finger bearing C-terminal region of MucR mediate oligomerization and DNA-binding, respectively. These features are convergent to those of xenogeneic silencers such as H-NS, MvaT, Lsr2 and Rok, which are mainly found in other lineages. Phylogenetic analysis of MucR homologs suggests an ancestral origin of MucR in alpha- and delta-proteobacteria. Multiple independent duplication and lateral gene transfer events contribute to the diversity and phyletic distribution of MucR. Finally, we posed questions which remain unexplored regarding the putative roles of MucR as a xenogeneic silencer and a general manager in balancing adaptation and regulatory integration in the pangenome context.

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The zinc-finger bearing xenogeneic silencer MucR in α-proteobacteria balances adaptation and regulatory integrity

Jiao

Zhang

et al. 2021

The ISME Journal

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Foreign AT-rich genes drive bacterial adaptation to new niches while challenging the existing regulation network. Here we report that MucR, a conserved regulator in α-proteobacteria, balances adaptation and regulatory integrity in Sinorhizobium fredii, a facultative microsymbiont of legumes. Chromatin immunoprecipitation sequencing coupled with transcriptomic data reveal that average transcription levels of both target and non-target genes, under free-living and symbiotic conditions, increase with their conservation levels. Targets involved in environmental adaptation and symbiosis belong to genus or species core and can be repressed or activated by MucR in a condition-dependent manner, implying regulatory integrations. However, most targets are enriched in strain-specific genes of lower expression levels and higher AT%. Within each conservation levels, targets have higher AT% and average transcription levels than non-target genes and can be further up-regulated in the mucR mutant. This is consistent with higher AT% of spacers between −35 and −10 elements of promoters for target genes, which enhances transcription. The MucR recruitment level linearly increases with AT% and the number of a flexible pattern (with periodic repeats of Ts) of target sequences. Collectively, MucR directly represses AT-rich foreign genes with predisposed high transcription potential while progressive erosions of its target sites facilitate regulatory integrations of foreign genes.

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Identifying the region responsible for Brucella abortus MucR higher-order oligomer formation and examining its role in gene regulation

Cited by 15 publications

References 75 publications

Different Impacts of MucR Binding to the babR and virB Promoters on Gene Expression in Brucella abortus 2308

Different Impacts of MucR Binding to the babR and virB Promoters on Gene Expression in Brucella abortus 2308

Ancestral zinc-finger bearing protein MucR in alpha-proteobacteria: A novel xenogeneic silencer?

The zinc-finger bearing xenogeneic silencer MucR in α-proteobacteria balances adaptation and regulatory integrity

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