Themes and Variations: Regulation of RpoN-Dependent Flagellar Genes across Diverse Bacterial Species

Tsang, Jennifer; Hoover, Timothy R.

doi:10.1155/2014/681754

Cited by 26 publications

(23 citation statements)

References 129 publications

(167 reference statements)

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“…In general, bacterial flagellar expression is highly regulated by different environmental conditions and is usually driven by a transcriptional and hierarchal cascade of genes in which full translation of the first component of the cascade is required to activate the expression of subsequent genes (Macnab 2003, Moisi et al 2009, Martinez et al 2010. Additionally, since the organization of the flagellar system appears to be evolutionarily conserved in Gram-negative bacteria (Tsang & Hoover 2014) Table 2. Piscirickettsia salmonis viability (%) in cell-free media.…”

Section: Discussionmentioning

confidence: 99%

Expression of flagellin and key regulatory flagellar genes in the non-motile bacterium Piscirickettsia salmonis

Carril

Gómez²,

Marshall³

2017

Dis. Aquat. Org.

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The Piscirickettsia salmonis genome was screened to evaluate potential flagellarelated open reading frames, as well as their genomic organization and eventual expression. A complete and organized set of flagellar genes was found for P. salmonis, although no structural flagellum has ever been reported for this bacterium. To gain further understanding, the hierarchical flagellar cascade described for Legionella pneumophila was used as a reference model for putative analysis in P. salmonis. Specifically, 5 of the most relevant genes from this cascade were chosen, including 3 regulatory genes (fleQ, triggers the cascade; fliA, regulates the σ28-coding gene; and rpoN, an RNA polymerase-dependent gene) and 2 terminal structural genes (flaA and flaB, flagellin and a flagellin-like protein, respectively). Kinetic experiments evaluated gene expressions over time, with P. salmonis assessed in 2 liquid, cell-free media and during infection of the SHK-1 fish cell line. Under all conditions, the 5 target genes were primarily expressed during early growth/infection and were differentially expressed when bacteria encountered environmental stress (i.e. a high-salt concentration). Intriguingly, the flagellin monomer was fully expressed under all growth conditions and was located near the bacterial membrane. While no structural flagellum was detected under any condition, the recombinant flagellin monomer induced a proinflammatory response in SHK-1 cells, suggesting a possible immunomodulatory function. The potential implications of these observations are discussed in the context of P. salmonis biology and pathogenic potential.

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Section: Discussionmentioning

confidence: 99%

Expression of flagellin and key regulatory flagellar genes in the non-motile bacterium Piscirickettsia salmonis

Carril

Gómez²,

Marshall³

2017

Dis. Aquat. Org.

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“…Despite remarkable morphological diversities of flagella in prokaryotes, their structures are alike and the assembly process is well conserved (Chevance and Hughes, ; Smith and Hoover, ). For bacteria harbouring a single polar flagellum, the flagellar genes are arranged into a four‐tiered transcriptionally regulatory hierarchy, as typified in V. cholerae (McCarter, ; Prouty et al ., ; Syed et al ., ; Tsang and Hoover, ). In brief as in http://onlinelibrary.wiley.com/doi/10.1111/mmi.12731/suppinfo, on the top is the master regulator FlrA or its homologue FleQ in Pseudomonas aeruginosa (class I), whose expression is σ 70 ‐dependent (Dasgupta et al ., ; Syed et al ., ; Dong and Mekalanos, ).…”

Section: Introductionmentioning

confidence: 99%

“…Despite remarkable morphological diversities of flagella in prokaryotes, their structures are alike and the assembly process is well conserved (Chevance and Hughes, 2008;Smith and Hoover, 2009). For bacteria harbouring a single polar flagellum, the flagellar genes are arranged into a four-tiered transcriptionally regulatory hierarchy, as typified in V. cholerae (McCarter, 2001;Prouty et al, 2001;Syed et al, 2009;Tsang and Hoover, 2014). In brief as in Fig.…”

Section: Introductionmentioning

confidence: 99%

“…Finally, secretion of the anti-σ 28 factor FlgM allows transcription of σ 28dependent genes, which encode the remaining flagellar components, including some flagellins, motor subunits, and chemotactic proteins. In V. cholerae, all of σ 54 , FlrA, FlrBC, and σ 28 are essential for motility (Klose and Mekalanos, 1998;Correa et al, 2000;Tsang and Hoover, 2014). Beyond these hierarchical regulators, there have been other proteins discovered in recent years having a role in complementing the regulatory networks.…”

Section: Introductionmentioning

confidence: 99%

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Effects of FlrBC on flagellar biosynthesis of Shewanella oneidensis

Shi

Gao

et al. 2014

Molecular Microbiology

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SummaryAs a most conserved complex molecular machine made up of a large number of structural subunits, the flagellum is under tight regulation by hierarchical arrangements. Although variations in polar flagellar systems are found, most of them are restricted to multiple-copy components, such as flagellins and stators. Therefore, these features are regarded to be peripheral relative to the comprehensive conservation. In this study, however, we present evidence to show that the difference in highly conserved polar flagellar systems can be surprisingly profound, even at the heart of the classical regulatory hierarchy. In Gram-negative Shewanella oneidensis, twocomponent system FlrBC, whose counterpart is essential for flagellar biosynthesis and motility by directly controlling expression of class III genes in polarly flagellated bacteria such as Vibrio cholerae, is dispensable for the process. The system directly controls expression of the flaA gene, encoding a flagellin of weak motility. We further show that the ratio of two flagellins, FlaA and FlaB, determines motility of a flagellum. More strikingly, overproduction of FlrC results in a peritrichously multi-flagellated phenotype, and FlrC is likely to function as an activator in its unphosphorylated form for transcription of the flaA gene, contrasting the previously characterized counterpart.

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“…Once the first flagellar structure is functional, FlbD becomes phosphorylated and activates E 54 to carry out transcription of the genes encoding the rod proteins, FlgH and FlgL (P and L rings, respectively), FlgE (the hook), and FliC (the filament). CtrA acts as a transcriptional activator when it is phosphorylated by the histidine kinase (HK) CckA and the histidine phosphotransferase ChpT (5)(6)(7). This signal transduction pathway is essential in Caulobacterales and Rhizobiales (8)(9)(10)(11).…”

mentioning

confidence: 99%

The Flagellar Set Fla2 in Rhodobacter sphaeroides Is Controlled by the CckA Pathway and Is Repressed by Organic Acids and the Expression of Fla1

et al. 2015

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Rhodobacter sphaeroides has two different sets of flagellar genes. Under the growth conditions commonly used in the laboratory, the expression of the fla1 set is constitutive, whereas the fla2 genes are not expressed. Phylogenetic analyses have previously shown that the fla1 genes were acquired by horizontal transfer from a gammaproteobacterium and that the fla2 genes are endogenous genes of this alphaproteobacterium. In this work, we characterized a set of mutants that were selected for swimming using the Fla2 flagella in the absence of the Fla1 flagellum (Fla2 ؉ strains). We determined that these strains have a single missense mutation in the histidine kinase domain of CckA. The expression of these mutant alleles in a Fla1؊ strain allowed fla2-dependent motility without selection. Motility of the Fla2 ؉ strains is also dependent on ChpT and CtrA. The mutant versions of CckA showed an increased autophosphorylation activity in vitro. Interestingly, we found that cckA is transcriptionally repressed by the presence of organic acids, suggesting that the availability of carbon sources could be a part of the signal that turns on this flagellar set. Evidence is presented showing that reactivation of fla1 gene expression in the Fla2؉ background strongly reduces the number of cells with Fla2 flagella. More than 40 genes are involved in the biogenesis and functioning of the bacterial flagellum. This structure has three major subcomponents, the basal body, the hook, and the filament. The basal body contains the export apparatus, an inner membrane ring (MS ring), a periplasmic ring (P ring), and, depending on the species, an outer membrane ring (L ring). The basal body also includes the flagellar motor and a rod that expands from the MS ring and crosses the L and P rings. The hook is the first extracellular structure that is assembled; it connects the basal body with the flagellar filament that is formed by thousands of flagellin subunits (reviewed in references 1-3).In most bacterial species, the expression of the flagellar genes is highly regulated and frequently follows a hierarchical order in which the late genes are expressed until the early genes, that are higher in the hierarchy, are expressed. At the top of the hierarchy, a transcriptional regulator is responsible for the expression of the genes required to assemble the early flagellar structures that are located in the cytoplasm (i.e., export apparatus), in the cytoplasmic membrane (i.e., MS ring), and, depending on the hierarchy, in the periplasm (i.e., P ring), the outer membrane (i.e., L ring), and the extracellular milieu (i.e., hook). Within this class, additional transcription factors are expressed. These proteins are required to transcribe the late genes, such as fliC (flagellin), fliD (filament cap), and fliS

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Themes and Variations: Regulation of RpoN-Dependent Flagellar Genes across Diverse Bacterial Species

Cited by 26 publications

References 129 publications

Expression of flagellin and key regulatory flagellar genes in the non-motile bacterium Piscirickettsia salmonis

Expression of flagellin and key regulatory flagellar genes in the non-motile bacterium Piscirickettsia salmonis

Effects of FlrBC on flagellar biosynthesis of Shewanella oneidensis

The Flagellar Set Fla2 in Rhodobacter sphaeroides Is Controlled by the CckA Pathway and Is Repressed by Organic Acids and the Expression of Fla1

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