The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing

Desai, Stuti K.; Winardhi, Ricksen S.; Saravanan, P.; Dykas, Michal Marcin; Yan, Jie; Kenney, Linda J.

doi:10.7554/elife.10747

Cited by 61 publications

(86 citation statements)

References 48 publications

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“…Antibiotics were added to final concentrations of 25 mg ml 21 kanamycin, 50 mg ml 21 ampicillin, 50 mg ml 21 spectinomycin and 12.5 mg ml 21 tetracycline, where necessary. Construction of strains by transduction and integration of gene cassettes were performed as described (Wilson et al, 1979;Miller, 1992;Diederich et al, 1992;Datsenko and Wanner, 2000). Plasmids used and constructed in this study are summarized in Supporting Information Table S1, and oligonucleotides are listed in Supporting Information Table S2.…”

Section: Bacterial Strains Plasmids and Mediamentioning

confidence: 99%

“…De-repression of H-NS repressed promoters in most cases is mediated locus-specifically by transcription regulators which presumably compete with H-NS for DNAbinding (Navarre et al, 2007;Stoebel et al, 2008). Displacement of H-NS has been shown to be mediated by regulators SsrB and Ler (Winardhi et al, 2014;Desai et al, 2016). Furthermore, H-NS-like and truncated H-NS protein variants which interact with H-NS can interfere with formation of repressive DNA-complexes by H-NS and alleviate repression (Williamson and Free, 2005;Doyle et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Interference of transcription across H‐NS binding sites and repression by H‐NS

Rangarajan

Schnetz

2018

Molecular Microbiology

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Nucleoid-associated protein H-NS represses transcription by forming extended DNA-H-NS complexes. Repression by H-NS operates mostly at the level of transcription initiation. Less is known about how DNA-H-NS complexes interfere with transcription elongation. In vitro H-NS has been shown to enhance RNA polymerase pausing and to promote Rho-dependent termination, while in vivo inhibition of Rho resulted in a decrease of the genome occupancy by H-NS. Here we show that transcription directed across H-NS binding regions relieves H-NS (and H-NS/StpA) mediated repression of promoters in these regions. Further, we observed a correlation of transcription across the H-NS-bound region and de-repression. The data suggest that the transcribing RNA polymerase is able to remodel the H-NS complex and/or dislodge H-NS from the DNA and thus relieve repression. Such an interference of transcription and H-NS mediated repression may imply that poorly transcribed AT-rich loci are prone to be repressed by H-NS, while efficiently transcribed loci escape repression.

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Section: Bacterial Strains Plasmids and Mediamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Interference of transcription across H‐NS binding sites and repression by H‐NS

Rangarajan

Schnetz

2018

Molecular Microbiology

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“… Unphosphorylated response regulators bind DNA and bend DNA to de‐repress H‐NS and relieve gene silencing. The upper panel shows a three dimensional reconstruction of SsrB (yellow) binding to the csgD (green) regulatory sequence (for details see Desai et al ., ) on which the repressor, H‐NS (blue), has formed a rigid nucleoprotein complex. Binding of SsrB introduces a bend in the csgD regulatory sequence, resulting in destabilization of the H‐NS filament and a relief of transcriptional silencing, as shown in the lower panel.…”

Section: Introductionmentioning

confidence: 99%

“…A). However, precise experiments involving single molecule (Desai et al ., ) or biochemical approaches (Will et al ., ) are lacking to determine whether DegU, like SsrB, bends the DNA to increase the affinity of ComK binding.…”

Section: Introductionmentioning

confidence: 99%

To ∼P or Not to ∼P? Non‐canonical activation by two‐component response regulators

Desai

Kenney

2016

Molecular Microbiology

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Summary Bacteria sense and respond to their environment through the use of two-component regulatory systems. The ability to adapt to a wide range of environmental stresses is directly related to the number of two-component systems an organism possesses. Recent advances in this area have identified numerous variations on the archetype systems that employ a sensor kinase and a response regulator. It is now evident that many orphan regulators that lack cognate kinases do not rely on phosphorylation for activation and new roles for unphosphorylated response regulators have been identified. The significance of recent findings and suggestions for further research are discussed.

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“…5 Systematic mutation of the single RR gene reveals that EsrA-EsrB is the most essential TCS in E. piscicida pathogenesis. 31 Like their counterparts SsrA, SsrB and SPI-2 in Salmonella, 32,33,34 EsrA and EsrB and the associated T3SS locus may be horizontally acquired and may have evolved to coordinate the expression of virulence and adaptation to host microenvironments by the reprogramming of ancestral genes unlinked to the T3SS locus. 6 Although the exact stimulus recognized by HK EsrA remains elusive, 35 EsrA-EsrB plays a key role in regulating the expression and secretion of T3SS and T6SS by directly binding to the promoters of T3SS genes and to that of EsrC, which further regulates the expression of other T3SS and T6SS genes in the bacterium.…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire inEdwardsiella piscicidaduring infection toward turbot

et al. 2017

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(2017) Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire in Edwardsiella piscicida during infection toward turbot, Virulence, 8:7, 1355-1377, DOI: 10.1080/21505594.2017 ABSTRACTEdwardsiella piscicida is the leading pathogen threatening worldwide aquaculture industries. The 2-component system (TCS) EsrA-EsrB is essential for the pathogenesis of this bacterium. However, little is known about the regulon and regulatory mechanism of EsrA-EsrB or about the factors that mediate the interaction of TCS with bacterial hosts. Here, our RNA-seq analysis indicated that EsrB strongly induces type III and type VI secretion systems (T3/T6SS) expression and that it modulates the expression of both physiology-and virulence-associated genes in E. piscicida grown in DMEM. EsrB binds directly to a highly conserved 18-bp DNA motif to regulate the expression of T3SS and other genes. EsrB/DMEM-activated genes include 3 known and 6 novel T3SS-dependent effectors. All these effector genes are highly induced by EsrB during the late stage of in vivo infection in fish. Furthermore, although in vivo colonization by the bacterium relies on EsrB and T3/T6SS expression, it does not require the expression of individual effectors other than EseJ. The mutant lacking these 9 effectors showed significant defects in in vivo colonization and virulence toward turbot, and, more importantly, a high level of protection against challenges by wild-type E. piscicida, suggesting that it may represent a promising live attenuated vaccine. Taken together, our data demonstrate that EsrB plays a global regulatory role in controlling physiologic responses and the expression of T3SS and its cognate effector genes. Our findings will facilitate further work on the mechanism of molecular pathogenesis of this bacterium during infection.

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The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing

Cited by 61 publications

References 48 publications

Interference of transcription across H‐NS binding sites and repression by H‐NS

Interference of transcription across H‐NS binding sites and repression by H‐NS

To ∼P or Not to ∼P? Non‐canonical activation by two‐component response regulators

Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire inEdwardsiella piscicidaduring infection toward turbot

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