Defining the function of OmpA in the Rcs stress response

Dekoninck, Kilian; Létoquart, Juliette; Laguri, Cédric; Demange, Pascal; Bevernaegie, Robin; Simorre, Jean-Pierre; Dehu, Olivia; Iorga, Bogdan I.; Elias, Benjamin; Cho, Seung-Hyun; Collet, Jean-François

doi:10.7554/elife.60861

Cited by 29 publications

(36 citation statements)

References 63 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We have also obtained evidence that OmpA competes with BamA for an interaction with DolP. A role of OmpA in buffering the function of an envelope stress factor has been reported (Dekoninck et al, 2020). We propose that, during envelope stress, the depletion of OmpA might enhance the interaction of DolP with BamA.…”

Section: Discussionsupporting

confidence: 54%

Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress

Ranava

Yang

Orenday-Tapia

et al. 2021

eLife

View full text Add to dashboard Cite

Integral outer membrane proteins (OMPs) are crucial for the maintenance of the proteobacterial envelope permeability barrier to some antibiotics and detergents. In Enterobacteria, envelope stress caused by unfolded OM proteins (OMPs) activates the sigmaE (σE) transcriptional response. σE upregulates OMP-biogenesis factors, including the b-barrel assembly machinery (BAM) that catalyzes OMP folding. Here we report that DolP (formerly YraP), a σE-upregulated and poorly understood OM lipoprotein, is crucial for fitness in cells that undergo envelope stress. We demonstrate that DolP interacts with the BAM complex by associating to OM-assembled BamA. We provide evidence that DolP is important for proper folding of BamA that overaccumulates in the OM, thus supporting OMP biogenesis and OM integrity. Notably, mid-cell recruitment of DolP had been linked to regulation of septal peptidoglycan remodelling by an unknown mechanism. We now reveal that, during envelope stress, DolP loses its association with the mid-cell, thereby suggesting a mechanistic link between envelope stress caused by impaired OMP biogenesis and the regulation of a late step of cell division.

show abstract

Section: Discussionsupporting

confidence: 54%

Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress

Ranava

Yang

Orenday-Tapia

et al. 2021

eLife

View full text Add to dashboard Cite

show abstract

“…Interestingly, OmpA was recently identified as a competitive binder of the lipoprotein RcsF ( 49 ), which we also identified as significantly upregulated during phage infection (FC +1.6). RcsF is a positive regulator of the Rcs stress response ( 50 ), of which we identified the significant upregulation of Rcs components RcsD (FC +1.7) during infection.…”

Section: Resultsmentioning

confidence: 64%

“…OmpA also seems to have a role in maintaining envelope integrity by linking the outer membrane to the peptidoglycan layer through the noncovalent linkage of its C-terminal domain to peptidoglycan ( 36 ). In addition to this activity, OmpA has a direct interaction with peptidoglycan stress sensory protein RcsF ( 49 ), which we also saw upregulated during infection (FC +1.6). Pal protein is also a mediator of outer membrane and peptidoglycan stability by forming a structural linkage between both layers ( 35 ).…”

Section: Discussionmentioning

confidence: 72%

See 1 more Smart Citation

Proteomic and Transcriptomic Analysis of Microviridae φX174 Infection Reveals Broad Upregulation of Host Escherichia coli Membrane Damage and Heat Shock Responses

et al. 2021

View full text Add to dashboard Cite

Measuring host-bacteriophage dynamics is an important approach to understanding bacterial survival functions and responses to infection. The model Microviridae bacteriophage φX174 is endemic to the human gut and has been studied for over 70 years, but the host response to infection has never been investigated in detail. To address this gap in our understanding of this important interaction within our microbiome, we have measured host Escherichia coli C proteomic and transcriptomic response to φX174 infection. We used mass spectrometry and RNA sequencing (RNA-seq) to identify and quantify all 11 φX174 proteins and over 1,700 E. coli proteins, enabling us to comprehensively map host pathways involved in φX174 infection. Most notably, we see significant host responses centered on membrane damage and remodeling, cellular chaperone and translocon activity, and lipoprotein processing, which we speculate is due to the peptidoglycan-disruptive effects of the φX174 lysis protein E on MraY activity. We also observe the massive upregulation of small heat shock proteins IbpA/B, along with other heat shock pathway chaperones, and speculate on how the specific characteristics of holdase protein activity may be beneficial for viral infections. Together, this study enables us to begin to understand the proteomic and transcriptomic host responses of E. coli to Microviridae infections and contributes insights to the activities of this important model host-phage interaction. IMPORTANCE A major part of the healthy human gut microbiome is the Microviridae bacteriophage, exemplified by the model φX174 phage, and their E. coli hosts. Although much has been learned from studying φX174 over the last half-century, until this work, the E. coli host response to infection has never been investigated in detail. We reveal the proteomic and transcriptomic pathways differentially regulated during the φX174 infection cycle and uncover the details of a coordinated cellular response to membrane damage that results in increased lipoprotein processing and membrane trafficking, likely due to the phage antibiotic-like lysis protein. We also reveal that small heat shock proteins IbpA/B are massively upregulated during infection and that these holdase chaperones are highly conserved across the domains of life, indicating that reliance on them is likely widespread across viruses.

show abstract

“…A recent study showed that OmpA is unlikely the vehicle allowing RcsF to reach the surface ( Dekoninck et al, 2020 ). Components of the Bam machinery, which assemble and localize OMPs, are needed to localize RcsF within the OMPs ( Cho et al, 2014 ; Konovalova et al, 2014 , 2016 ; Dekoninck et al, 2020 ; Rodríguez-Alonso et al, 2020 ). Rodríguez-Alonso et al reported the crystal structure of the key BAM component BamA in complex with RcsF and revealed how BamA interacts with RcsF.…”

Section: An Overview Of the Rcs Systemmentioning

confidence: 99%

The Rcs System in Enterobacteriaceae: Envelope Stress Responses and Virulence Regulation

2021

View full text Add to dashboard Cite

The bacterial cell envelope is a protective barrier at the frontline of bacterial interaction with the environment, and its integrity is regulated by various stress response systems. The Rcs (regulator of capsule synthesis) system, a non-orthodox two-component regulatory system (TCS) found in many members of the Enterobacteriaceae family, is one of the envelope stress response pathways. The Rcs system can sense envelope damage or defects and regulate the transcriptome to counteract stress, which is particularly important for the survival and virulence of pathogenic bacteria. In this review, we summarize the roles of the Rcs system in envelope stress responses (ESRs) and virulence regulation. We discuss the environmental and intrinsic sources of envelope stress that cause activation of the Rcs system with an emphasis on the role of RcsF in detection of envelope stress and signal transduction. Finally, the different regulation mechanisms governing the Rcs system’s control of virulence in several common pathogens are introduced. This review highlights the important role of the Rcs system in the environmental adaptation of bacteria and provides a theoretical basis for the development of new strategies for control, prevention, and treatment of bacterial infections.

show abstract

Defining the function of OmpA in the Rcs stress response

Cited by 29 publications

References 63 publications

Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress

Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress

Proteomic and Transcriptomic Analysis of Microviridae φX174 Infection Reveals Broad Upregulation of Host Escherichia coli Membrane Damage and Heat Shock Responses

The Rcs System in Enterobacteriaceae: Envelope Stress Responses and Virulence Regulation

Contact Info

Product

Resources

About