Stress-Induced Remodeling of the Bacterial Proteome

Guo, Monica S.; Gross, Carol A.

doi:10.1016/j.cub.2014.03.023

Cited by 92 publications

(101 citation statements)

References 196 publications

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“…Surprisingly, we found that the Pup ligase has a Pup-independent role in sporulation. P rotein homeostasis is a tightly regulated and critically important phenomenon in bacterial physiology (1). It is thought to be particularly complex in actinobacteria, which have both the canonical proteolytic machinery of prokaryotes and 20S proteasomes analogous to those of eukaryotes that are accompanied by a functional equivalent of ubiquitin known as the prokaryotic ubiquitin-like protein (Pup) (2)(3)(4)(5)(6)(7).…”

Section: Importancementioning

confidence: 99%

Genetic and Proteomic Analyses of Pupylation in Streptomyces coelicolor

et al. 2015

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Pupylation is a posttranslational modification peculiar to actinobacteria wherein proteins are covalently modified with a small protein called the prokaryotic ubiquitin-like protein (Pup). Like ubiquitination in eukaryotes, this phenomenon has been associated with proteasome-mediated protein degradation in mycobacteria. Here, we report studies of pupylation in a streptomycete that is phylogentically related to mycobacteria. We constructed mutants of Streptomyces coelicolor lacking PafA (Pup ligase), the proteasome, and the Pup-proteasome system. We found that these mutants share a high susceptibility to oxidative stress compared to that of the wild-type strain. Remarkably, we found that the pafA null mutant has a sporulation defect not seen in strains lacking the Pup-proteasome system. In proteomics experiments facilitated by an affinity-tagged variant of Pup, we identified 110 pupylated proteins in S. coelicolor strains having and lacking genes encoding the 20S proteasome. Our findings shed new light on this unusual posttranslational modification and its role in Streptomyces physiology. IMPORTANCEThe presence of 20S proteasomes reminiscent of those in eukaryotes and a functional equivalent of ubiquitin, known as the prokaryotic ubiquitin-like protein (Pup), in actinobacteria have motivated reevaluations of protein homeostasis in prokaryotes. Though the Pup-proteasome system has been studied extensively in mycobacteria, it is much less understood in streptomycetes, members of a large genus of actinobacteria known for highly choreographed life cycles in which phases of morphological differentiation, sporulation, and secondary metabolism are often regulated by protein metabolism. Here, we define constituents of the pupylome in Streptomyces coelicolor for the first time and present new evidence that links pupylation and the oxidative stress response in this bacterium. Surprisingly, we found that the Pup ligase has a Pup-independent role in sporulation.

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Section: Importancementioning

confidence: 99%

Genetic and Proteomic Analyses of Pupylation in Streptomyces coelicolor

et al. 2015

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“…The transcriptional and translational control of stress response is a well-known phenomenon and forms the basis of dramatic cellular reprogramming in response to environmental stress (reviewed in Chung, 2006;Guo and Gross, 2014;Shimizu, 2013). An elaborate interconnected network of pathways is involved in regulating translation in response to varied stresses such as nutrient deprivation, pH, ionic strength, and temperature (Wilson and Nierhaus, 2007).…”

Section: Figmentioning

confidence: 99%

“…While it is recognized that certain common phenomena underlie generalized stress responses (Guo and Gross, 2014), studies aimed at identifying central stress response proteins could only conclude that every stress response has a specialized mechanism of action. Cross-stress protection, the ability of one stress condition to provide protection against other stressors, also suggests a central control of stress response.…”

mentioning

confidence: 99%

“…The bacterial stringent response has been used as a template to understand global regulatory processes (Durfee et al, 2008). It was found that the fast and accurate responses to stress involve specific proteolysis and broad transcriptional remodeling mediated by various sigma factors, Lon/Clp proteases, and Two Component Systems (TCS) (Guo and Gross, 2014). Stress-induced responses include changes in membrane composition, motility, modification of proteins, and their transcription and translation machineries (Caspeta et al, 2009;Dupont et al, 2007;Moll and Engelberg-Kulka, 2012;Nachin et al, 2005;Wilson and Nierhaus, 2007).…”

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confidence: 99%

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A Network Biology Approach to Decipher Stress Response in Bacteria UsingEscherichia coliAs a Model

Nagar

Aggarwal

Joon

et al. 2016

OMICS: A Journal of Integrative Biology

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The development of drug-resistant pathogenic bacteria poses challenges to global health for their treatment and control. In this context, stress response enables bacterial populations to survive extreme perturbations in the environment but remains poorly understood. Specific modules are activated for unique stressors with few recognized global regulators. The phenomenon of cross-stress protection strongly suggests the presence of central proteins that control the diverse stress responses. In this work, Escherichia coli was used to model the bacterial stress response. A Protein-Protein Interaction Network was generated by integrating differentially expressed genes in eight stress conditions of pH, temperature, and antibiotics with relevant gene ontology terms. Topological analysis identified 24 central proteins. The well-documented role of 16 central proteins in stress indicates central control of the response, while the remaining eight proteins may have a novel role in stress response. Cluster analysis of the generated network implicated RNA binding, flagellar assembly, ABC transporters, and DNA repair as important processes during response to stress. Pathway analysis showed crosstalk of Two Component Systems with metabolic processes, oxidative phosphorylation, and ABC transporters. The results were further validated by analysis of an independent cross-stress protection dataset. This study also reports on the ways in which bacterial stress response can progress to biofilm formation. In conclusion, we suggest that drug targets or pathways disrupting bacterial stress responses can potentially be exploited to combat antibiotic tolerance and multidrug resistance in the future.

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“…It is in this compartment where most of the perception of the bacterial surroundings takes place. Sensory devices, usually periplasmic-protruding inner-membrane histidine kinases or antisigma factors, detect changes in the environment and transduce this information to cytoplasmic effectors, usually transcriptional regulators (2,3). This simple array provides an efficient and rapid response to modulate the expression of factors required to cope with a continuously challenging environment.…”

mentioning

confidence: 99%

Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis

Pezza

Pontel

López

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Copper homeostasis is essential for bacterial pathogen fitness and infection, and has been the focus of a number of recent studies. In Salmonella, envelope protection against copper overload and macrophage survival depends on CueP, a major copper-binding protein in the periplasm. This protein is also required to deliver the metal ion to the Cu/Zn superoxide dismutase SodCII. The Salmonella-specific CueP-coding gene was originally identified as part of the Cue regulon under the transcriptional control of the cytoplasmic copper sensor CueR, but its expression differs from the rest of CueR-regulated genes. Here we show that cueP expression is controlled by the concerted action of CueR, which detects the presence of copper in the cytoplasm, and by CpxR/CpxA, which monitors envelope stress. Copper-activated CueR is necessary for the appropriate spatial arrangement of the −10 and −35 elements of the cueP promoter, and CpxR is essential to recruit the RNA polymerase. The integration of two ancestral sensory systems—CueR, which provides signal specificity, and CpxR/CpxA, which detects stress in the bacterial envelope—restricts the expression of this periplasmic copper resistance protein solely to cells encountering surplus copper that disturbs envelope homeostasis, emulating the role of the CusR/CusS regulatory system present in other enteric bacteria.

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Stress-Induced Remodeling of the Bacterial Proteome

Cited by 92 publications

References 196 publications

Genetic and Proteomic Analyses of Pupylation in Streptomyces coelicolor

Genetic and Proteomic Analyses of Pupylation in Streptomyces coelicolor

A Network Biology Approach to Decipher Stress Response in Bacteria UsingEscherichia coliAs a Model

Compartment and signal-specific codependence in the transcriptional control of Salmonella periplasmic copper homeostasis

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