DNA-Binding and Transcription Activation by Unphosphorylated Response Regulator AgrR From Cupriavidus metallidurans Involved in Silver Resistance

Ali, Muntasir; Provoost, Ann; Mijnendonckx, Kristel; Charlier, Daniël

doi:10.3389/fmicb.2020.01635

Cited by 12 publications

(7 citation statements)

References 116 publications

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“…Interestingly, we observed considerable variation in the expression levels of cop 1 genes with similar consensus motifs. This could indicate that these small variations of the operator sequence have large effects on their interaction with regulatory proteins (e.g., CopR 1 ), as was shown for binding of response regulator AgrR in C. metallidurans NA4 [ 147 ], or that additional regulatory factors are involved. In addition, this motif was also detected upstream of the pTSSs of cusA , cupA , cupC , and copB 2 (FIMO; p < 0.001 [ 148 ]).…”

Section: Resultsmentioning

confidence: 92%

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Maertens

Leys

Matroule

2020

Genes

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Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA-sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper-specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine-sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re-annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post-transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.

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Section: Resultsmentioning

confidence: 92%

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Maertens

Leys

Matroule

2020

Genes

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“…This feedback mechanism involving modulation of the ability of SKs to regulate the concentration of phosphorylated RRs plays a critical role in the TCS-mediated response [109]. While most RRs are activated by phosphorylation [109], unphosphorylated CsgD of Salmonella enterica [110] and AgrR of Cupriavidus metallidurans are the active forms [111]. Despite a nearly 19-fold higher abundance of PprA in Δ plaF , we have not observed an increased abundance of phosphorylated PprB, yet transcription of bap and cup was upregulated, while that for pqs and tad from the pprB regulon was not upregulated.…”

Section: Discussionmentioning

confidence: 99%

Virulence adaptation ofPseudomonas aeruginosaphospholipase mutant with altered membrane phospholipid composition

Caliskan

Poschmann

Gudzuhn

et al. 2022

Preprint

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Membrane protein and phospholipid (PL) composition changes in response to environmental cues and during infections. Covalent modification and remodelling of the acyl chain length of PLs is an important bacterial adaptation mechanism. However, little is known about which bacterial pathways are regulated in response to altered PL composition. Here, we showed that P. aeruginosa phospholipase A, PlaF, which modulates membrane PL composition, is important for biofilm biogenesis, and we performed whole-cell quantitative proteomics of P. aeruginosa wild-type and delta plaF biofilms to identify pathways regulated by PlaF. The results revealed profound alterations in the abundance of several two-component systems (TCSs), including accumulation of PprAB, which controls the transition to biofilm. Furthermore, a unique phosphorylation pattern of transcriptional regulators, transporters and metabolic enzymes, as well as differential production of seven proteases, in delta plaF, indicate that PlaF-mediated virulence adaptation involves complex transcriptional and posttranscriptional regulation. Moreover, proteomics revealed the depletion of pyoverdine-mediated iron uptake pathway proteins in delta plaF, which agrees with the decreased concentrations of extracellular pyoverdine and intracellular iron and is likely responsible for its prolonged lag growth phase, presumably due to reduced iron uptake. Conversely, the accumulation of proteins from alternative iron-uptake systems in delta plaF suggests that PlaF may function as a switch between different iron-acquisition pathways. The observation that ∆plaF accumulates PL-acyl chain modifying and PL synthesis enzymes reveals novel insights into the role of PlaF for membrane PL homeostasis. Although the precise mechanism by which PlaF simultaneously affects multiple pathways remains to be elucidated, we suggest that PlaF-catalyses the degradation of PLs which then serve as a signal that is amplified by proteins of two-component, phosphorylation and proteolytic degradation systems to elicit the global adaptive response in P. aeruginosa.

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“…7). Although autoregulation of TCS gene expression is found in several TCSs and their regulators have also been shown to bind to their cognate promoter DNA in their non-phosphorylated states such as AgrR in Cupriavidus metallidurans and the orphan response regulator in Streptomyces coelicolor (Roy et al, 1991;Holman et al, 1994;Liu et al, 1997;Hayde et al, 2002;Wang et al, 2009;Ali et al, 2020), gene transcription without the presence of their cognate sensor kinase is still rare. Interestingly, our study clearly showed that FleR plays a critical role in the activation of its own expression even in the absence of its kinase pair FleS.…”

Section: Discussionmentioning

confidence: 99%

A Two-Component System FleS/FleR Regulates Multiple Virulence-Related Traits inPseudomonas aeruginosa

Zhou

Huang

Feng

et al. 2021

Preprint

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Microorganisms commonly use two-component systems (TCSs) to detect specific environmental changes and respond accordingly for their own benefit. However, the regulatory mechanisms and physiological roles of a majority of TCSs are still elusive. In this study, we focused on a previously predicted TCS FleS/FleR in Pseudomonas aeruginosa to systematically investigate its regulation and physiological roles. Loss of fleS or fleR or both genes led to decreased biofilm formation and attenuated motility in PAO1, which could be restored by heterologously complementation of FleR but not FleS, confirming that the sensor kinase FleS and the response regulator FleR constitute a TCS pair. To determine the regulatory spectrum of this TCS, we conducted transcriptome sequencing and comparison between the wild-type strain and the fleR deletion mutant. The result showed that the TCS regulates about 440 genes including most of them are involved in the virulence-related pathways, e.g. siderophore biosynthesis, pyocyanin biosynthesis, type III/VI secretion systems, c-di-GMP metabolism, flagellar assembly etc. In addition to its roles in controlling biofilm formation and motility we have already shown, FleR was demonstrated to regulate the production of virulence factors such as pyocyanin and elastase, mediate stress response to SDS, and autoregulate its own expression. Moreover, EMSA assays revealed that FleR regulates flagellum biosynthesis genes flgBCDE, flgFGHIJKL, filC, which are essential for the bacterial motility, by directly interacting with their promoters. Taken together, these results expanded our understanding on the biological roles of FleS/FleR and provided new insights on its regulatory mechanisms.

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DNA-Binding and Transcription Activation by Unphosphorylated Response Regulator AgrR From Cupriavidus metallidurans Involved in Silver Resistance

Cited by 12 publications

References 116 publications

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Virulence adaptation ofPseudomonas aeruginosaphospholipase mutant with altered membrane phospholipid composition

A Two-Component System FleS/FleR Regulates Multiple Virulence-Related Traits inPseudomonas aeruginosa

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