scholarly journals A Polar Flagellar Transcriptional Program Mediated by Diverse Two-Component Signal Transduction Systems and Basal Flagellar Proteins Is Broadly Conserved in Polar Flagellates

mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Peter M. Burnham ◽  
William P. Kolar ◽  
David R. Hendrixson
Keyword(s):  
Signal Transduction ◽  
Gene Transcription ◽  
Regulatory System ◽  
Transcriptional Program ◽  
Content Type ◽  
Regulatory Processes ◽  
Two Component ◽  
Two Component Signal Transduction ◽  
Flagellar Biogenesis ◽  
Signal Transduction Systems

ABSTRACT Bacterial flagella are rotating nanomachines required for motility. Flagellar gene expression and protein secretion are coordinated for efficient flagellar biogenesis. Polar flagellates, unlike peritrichous bacteria, commonly order flagellar rod and hook gene transcription as a separate step after production of the MS ring, C ring, and flagellar type III secretion system (fT3SS) core proteins that form a competent fT3SS. Conserved regulatory mechanisms in diverse polar flagellates to create this polar flagellar transcriptional program have not been thoroughly assimilated. Using in silico and genetic analyses and our previous findings in Campylobacter jejuni as a foundation, we observed a large subset of Gram-negative bacteria with the FlhF/FlhG regulatory system for polar flagellation to possess flagellum-associated two-component signal transduction systems (TCSs). We present data supporting a general theme in polar flagellates whereby MS ring, rotor, and fT3SS proteins contribute to a regulatory checkpoint during polar flagellar biogenesis. We demonstrate that Vibrio cholerae and Pseudomonas aeruginosa require the formation of this regulatory checkpoint for the TCSs to directly activate subsequent rod and hook gene transcription, which are hallmarks of the polar flagellar transcriptional program. By reprogramming transcription in V. cholerae to more closely follow the peritrichous flagellar transcriptional program, we discovered a link between the polar flagellar transcription program and the activity of FlhF/FlhG flagellar biogenesis regulators in which the transcriptional program allows polar flagellates to continue to produce flagella for motility when FlhF or FlhG activity may be altered. Our findings integrate flagellar transcriptional and biogenesis regulatory processes involved in polar flagellation in many species. IMPORTANCE Relative to peritrichous bacteria, polar flagellates possess regulatory systems that order flagellar gene transcription differently and produce flagella in specific numbers only at poles. How transcriptional and flagellar biogenesis regulatory systems are interlinked to promote the correct synthesis of polar flagella in diverse species has largely been unexplored. We found evidence for many Gram-negative polar flagellates encoding two-component signal transduction systems with activity linked to the formation of flagellar type III secretion systems to enable production of flagellar rod and hook proteins at a discrete, subsequent stage during flagellar assembly. This polar flagellar transcriptional program assists, in some manner, the FlhF/FlhG flagellar biogenesis regulatory system, which forms specific flagellation patterns in polar flagellates in maintaining flagellation and motility when activity of FlhF or FlhG might be altered. Our work provides insight into the multiple regulatory processes required for polar flagellation.

scholarly journals Two-Component Signal Transduction Systems in the Human Pathogen Streptococcus agalactiae

2020 ◽  
Vol 88 (7) ◽  
Author(s):  
Lamar Thomas ◽  
Laura Cook
Keyword(s):  
Signal Transduction ◽  
Streptococcus Agalactiae ◽  
Metabolic Regulation ◽  
Invasive Infection ◽  
Older Individuals ◽  
Content Type ◽  
Two Component ◽  
Two Component Signal Transduction ◽  
Group B ◽  
Signal Transduction Systems

ABSTRACT Streptococcus agalactiae (group B Streptococcus [GBS]) is an important cause of invasive infection in newborns, maternal women, and older individuals with underlying chronic illnesses. GBS has many mechanisms to adapt and survive in its host, and these mechanisms are often controlled via two-component signal transduction systems. In GBS, more than 20 distinct two-component systems (TCSs) have been classified to date, consisting of canonical TCSs as well as orphan and atypical sensors and regulators. These signal transducing systems are necessary for metabolic regulation, resistance to antibiotics and antimicrobials, pathogenesis, and adhesion to the mucosal surfaces to colonize the host. This minireview discusses the structures of these TCSs in GBS as well as how selected systems regulate essential cellular processes such as survival and colonization. GBS contains almost double the number of TCSs compared to the closely related Streptococcus pyogenes and Streptococcus pneumoniae, and while research on GBS TCSs has been increasing in recent years, no comprehensive reviews of these TCSs exist, making this review especially relevant.

scholarly journals The ChrSA and HrrSA Two-Component Systems Are Required for Transcriptional Regulation of thehemAPromoter in Corynebacterium diphtheriae

2016 ◽  
Vol 198 (18) ◽  
pp. 2419-2430 ◽  
Author(s):  
Jonathan M. Burgos ◽  
Michael P. Schmitt
Keyword(s):  
Signal Transduction ◽  
Kinase Activity ◽  
Content Type ◽  
Component Systems ◽  
Two Component ◽  
Two Component Signal Transduction ◽  
Two Component Systems ◽  
Signal Transduction Systems

ABSTRACTCorynebacterium diphtheriaeutilizes heme and hemoglobin (Hb) as iron sources for growth in low-iron environments. InC. diphtheriae, the two-component signal transduction systems (TCSs) ChrSA and HrrSA are responsive to Hb levels and regulate the transcription of promoters forhmuO,hrtAB, andhemA. ChrSA and HrrSA activate transcription at thehmuOpromoter and repress transcription athemAin an Hb-dependent manner. In this study, we show that HrrSA is the predominant repressor athemAand that its activity results in transcriptional repression in the presence and absence of Hb, whereas repression ofhemAby ChrSA is primarily responsive to Hb. DNA binding studies showed that both ChrA and HrrA bind to thehemApromoter region at virtually identical sequences. ChrA binding was enhanced by phosphorylation, while binding to DNA by HrrA was independent of its phosphorylation state. ChrA and HrrA are phosphorylatedin vitroby the sensor kinase ChrS, whereas no kinase activity was observed with HrrSin vitro. Phosphorylated ChrA was not observedin vivo, even in the presence of Hb, which is likely due to the instability of the phosphate moiety on ChrA. However, phosphorylation of HrrA was observedin vivoregardless of the presence of the Hb inducer, and genetic analysis indicates that ChrS is responsible for most of the phosphorylation of HrrAin vivo. Phosphorylation studies strongly suggest that HrrS functions primarily as a phosphatase and has only minimal kinase activity. These findings collectively show a complex mechanism of regulation at thehemApromoter, where both two-component systems act in concert to optimize expression of heme biosynthetic enzymes.IMPORTANCEUnderstanding the mechanism by which two-component signal transduction systems function to respond to environmental stimuli is critical to the study of bacterial pathogenesis. The current study expands on the previous analyses of the ChrSA and HrrSA TCSs in the human pathogenC. diphtheriae. The findings here underscore the complex interactions between the ChrSA and HrrSA systems in the regulation of thehemApromoter and demonstrate how the two systems complement one another to refine and control transcription in the presence and absence of Hb.

scholarly journals Global Regulation of Gene Expression by ArlRS, a Two-Component Signal Transduction Regulatory System of Staphylococcus aureus

2005 ◽  
Vol 187 (15) ◽  
pp. 5486-5492 ◽  
Author(s):  
Xudong Liang ◽  
Li Zheng ◽  
Christina Landwehr ◽  
Dwayne Lunsford ◽  
David Holmes ◽  
...  
Keyword(s):  
Signal Transduction ◽  
Staphylococcus Aureus ◽  
Microarray Data ◽  
Regulation Of Gene Expression ◽  
Regulatory System ◽  
Transcriptional Regulators ◽  
Microarray Technology ◽  
Two Component ◽  
Two Component Signal Transduction ◽  
Signal Transduction Systems

ABSTRACT Staphylococcus aureus expresses various cell wall-associated and extracellular virulence factors, coordinately controlled by different two-component signal transduction systems and transcriptional regulators. In this study, we used microarray technology to identify the genes regulated by ArlR. The microarray data indicate that ArlR functions as a positive regulator and also as a negative repressor to directly and/or indirectly mediate the expression of at least 114 genes involved in different functions, including autolysis, cell division, growth, and pathogenesis.

scholarly journals A Regulatory Checkpoint during Flagellar Biogenesis in Campylobacter jejuni Initiates Signal Transduction To Activate Transcription of Flagellar Genes

mBio ◽  
2013 ◽  
Vol 4 (5) ◽  
Author(s):  
Joseph M. Boll ◽  
David R. Hendrixson
Keyword(s):  
Signal Transduction ◽  
Campylobacter Jejuni ◽  
Gene Transcription ◽  
Type Iii Secretion ◽  
Secretion System ◽  
Flagellar Gene ◽  
Content Type ◽  
Regulatory Systems ◽  
Two Component ◽  
Flagellar Biogenesis

ABSTRACTMany polarly flagellated bacteria require similar two-component regulatory systems (TCSs) and σ54to activate transcription of genes essential for flagellar motility. Herein, we discovered that in addition to the flagellar type III secretion system (T3SS), theCampylobacter jejuniflagellar MS ring and rotor are required to activate the FlgSR TCS. Mutants lacking the FliF MS ring and FliG C ring rotor proteins were as defective as T3SS mutants in FlgSR- and σ54-dependent flagellar gene expression. Also, FliF and FliG required each other for stability, which is mediated by atypical extensions to the proteins. A FliF mutant that presumably does not interact with the T3SS protein FlhA did not support flagellar gene transcription, suggesting that FliF-T3SS interactions are essential to generate a signal sensed by the cytoplasmic FlgS histidine kinase. Furthermore, the flagellar T3SS was required for FlgS to immunoprecipitate with FliF and FliG. We propose a model whereby the flagellar T3SS facilitates FliF and FliG multimerization into the MS ring and rotor. As a result, these flagellar structures form a cytoplasmic complex that interacts with and is sensed by FlgS. The synthesis of these structures appears to be a regulatory checkpoint in flagellar biogenesis that the FlgS kinase monitors to initiate signal transduction that activates σ54and expression of genes required for the next stage of flagellation. Given that other polar flagellates have flagellar transcriptional hierarchies that are organized similarly as inC. jejuni, this regulatory checkpoint may exist in a broad range of bacteria to influence similar TCSs and flagellar gene transcription.IMPORTANCEDespite the presence of numerous two-component regulatory systems (TCSs) in bacteria, direct signals sensed by TCSs to activate signal transduction are known for only a minority. Polar flagellates, includingPseudomonas,Vibrio,Helicobacter, andCampylobacterspecies, require a similar TCS and σ54for flagellar gene transcription, but the activating signals for these TCSs are unknown. We explored signals that activate theCampylobacter jejuniFlgSR TCS to initiate σ54-dependent flagellar gene transcription. Our discoveries suggest that the FlgS histidine kinase monitors the formation of the flagellar type III secretion system and the surrounding MS and C rings. The synthesis of these structures creates a regulatory checkpoint in flagellar biogenesis that is sensed by FlgS to ensure proper transcription of the next set of genes for subsequent steps in flagellation. Given the conservation of flagellar-associated TCSs and transcriptional cascades in polar flagellates, this regulatory checkpoint in flagellar biogenesis likely impacts flagellation in a broad range of bacteria.

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