Synergistic action of SPI-1 gene expression in Salmonella enterica serovar typhimurium through transcriptional crosstalk with the flagellar system

Hamed, Selwan; Wang, Xiaoyi; Shawky, Riham M.; Emara, Mohamed; Aldridge, Philip D.; Rao, Christopher V.

doi:10.1186/s12866-019-1583-7

Cited by 19 publications

(29 citation statements)

References 47 publications

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“…SPI1 encodes a type III secretion system (T3SS1), required for invasion of intestinal epithelial cells and gut inflammation, as well as several transcriptional regulators 8 . The SPI1 regulon is induced in the gut 9 – 11 , via mechanisms that are not fully understood, or under certain in vitro growth conditions 12 – 14 , which has enabled characterization of many of the players and revealed transcriptional cross talk with motility genes 15 – 24 . The SPI1-encoded transcription factors HilA and HilD are the dominant regulators of SPI1 expression.…”

Section: Introductionmentioning

confidence: 99%

“…HilD activates HilA 16 , 25 and also directly activates transcription of the flagellar master operon flhDC by binding upstream of the P5 promoter 21 . In fact, many flagellar proteins also target HilA or HilD 14 , 26 . Both SPI1 and flagellar genes exhibit bistable expression, i.e, expressing and non-expressing bacteria coexist in the same populations.…”

Section: Introductionmentioning

confidence: 99%

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Regulatory protein HilD stimulates Salmonella Typhimurium invasiveness by promoting smooth swimming via the methyl-accepting chemotaxis protein McpC

et al. 2021

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In the enteric pathogen Salmonella enterica serovar Typhimurium, invasion and motility are coordinated by the master regulator HilD, which induces expression of the type III secretion system 1 (T3SS1) and motility genes. Methyl-accepting chemotaxis proteins (MCPs) detect specific ligands and control the direction of the flagellar motor, promoting tumbling and changes in direction (if a repellent is detected) or smooth swimming (in the presence of an attractant). Here, we show that HilD induces smooth swimming by upregulating an uncharacterized MCP (McpC), and this is important for invasion of epithelial cells. Remarkably, in vitro assays show that McpC can suppress tumbling and increase smooth swimming in the absence of exogenous ligands. Expression of mcpC is repressed by the universal regulator H-NS, which can be displaced by HilD. Our results highlight the importance of smooth swimming for Salmonella Typhimurium invasiveness and indicate that McpC can act via a ligand-independent mechanism when incorporated into the chemotactic receptor array.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Regulatory protein HilD stimulates Salmonella Typhimurium invasiveness by promoting smooth swimming via the methyl-accepting chemotaxis protein McpC

et al. 2021

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“…Flagellar gene expression is bimodal in S. enterica (3–9). Under certain growth conditions, some cells express the flagellar genes whereas others do not.…”

Section: Discussionmentioning

confidence: 99%

“…Multiple studies have observed bimodal expression of the flagellar genes in S. enterica (3–9). As a brief background, the flagellar promoters can be grouped into three hierarchical classes based on how they are temporally activated (10, 11).…”

Section: Introductionmentioning

confidence: 99%

Two tandem mechanisms control bimodal expression of the flagellar genes inSalmonella enterica

Wang

Koirala

Aldridge

et al. 2019

Preprint

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ABSTRACTFlagellar gene expression is bimodal in Salmonella enterica. Under certain growth conditions, some cells express the flagellar genes whereas others do not. This results in mixed populations of motile and non-motile cells. In the present study, we found that two independent mechanisms control bimodal expression of the flagellar genes. One was previously found to result from a double negative-feedback loop involving the flagellar regulators YdiV and FliZ. This feedback loop governs bimodal expression of class 2 genes. In this work, a second mechanism was found to govern bimodal expression of class 3 genes. In particular, class 3 gene expression is still bimodal even when class 2 gene expression is not. Using a combination of experimental and modeling approaches, we found that class 3 bimodalilty results from the σ28-FlgM developmental checkpoint.IMPORTANCEMany bacterial use flagella to swim in liquids and swarm over surface. In Salmonella enterica, over fifty genes are required to assemble flagella. The expression of these genes is tightly regulated. Previous studies have found that flagella gene expression is bimodal in S. enterica, which means that only a fraction of cells express flagellar genes and are motile. In the present study, we found that two separate mechanisms induce this bimodal response. One mechanism, which was previously identified, tunes the fraction of motile cells in response to nutrients. The other results from a developmental checkpoint that couples flagellar gene expression to flagellar assembly. Collectively, these results further our understanding of how flagellar gene expression is regulated in S. enterica.

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“…In previous work, we found that acetate and nutrients, provided as yeast extract, synergistically induce SPI-1 gene expression [ 13 ]. Both acetate and yeast extract are individually capable of inducing SPI-1 gene expression.…”

Section: Introductionmentioning

confidence: 99%

HilE is required for synergistic activation of SPI-1 gene expression in Salmonella enterica serovar Typhimurium

et al. 2021

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Background Salmonella enterica serovar Typhimurium is an intestinal pathogen capable of infecting a wide range of animals. It initiates infection by invading intestinal epithelial cells using a type III secretion system encoded within Salmonella pathogenicity island 1 (SPI-1). The SPI-1 genes are regulated by multiple interacting transcription factors. The master regulator is HilD. HilE represses SPI-1 gene expression by binding HilD and preventing it from activating its target promoters. Previous work found that acetate and nutrients synergistically induce SPI-1 gene expression. In the present study, we investigated the role of HilE, nominally a repressor of SPI-1 gene expression, in mediating this response to acetate and nutrients. Results HilE is necessary for activation of SPI-1 gene expression by acetate and nutrients. In mutants lacking hilE, acetate and nutrients no longer increase SPI-1 gene expression but rather repress it. This puzzling response is not due to the BarA/SirA two component system, which governs the response to acetate. To identify the mechanism, we profiled gene expression using RNAseq in the wild type and a ΔhilE mutant under different growth conditions. Analysis of these data suggested that the Rcs system, which regulates gene expression in response to envelope stress, is involved. Consistent with this hypothesis, acetate and nutrients were able to induce SPI-1 gene expression in mutants lacking hilE and the Rcs system. Conclusions While the exact mechanism is unknown, these results demonstrate the HilE, nominally a repressor of SPI-1 gene expression, can also function as an activator under the growth conditions investigated. Collectively, these results provide new insights regarding SPI-1 gene regulation and demonstrate that HilE is more complex than initially envisioned.

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Synergistic action of SPI-1 gene expression in Salmonella enterica serovar typhimurium through transcriptional crosstalk with the flagellar system

Cited by 19 publications

References 47 publications

Regulatory protein HilD stimulates Salmonella Typhimurium invasiveness by promoting smooth swimming via the methyl-accepting chemotaxis protein McpC

Regulatory protein HilD stimulates Salmonella Typhimurium invasiveness by promoting smooth swimming via the methyl-accepting chemotaxis protein McpC

Two tandem mechanisms control bimodal expression of the flagellar genes inSalmonella enterica

HilE is required for synergistic activation of SPI-1 gene expression in Salmonella enterica serovar Typhimurium

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