Roles of Lon protease and its substrate MarA during sodium salicylate-mediated growth reduction and antibiotic resistance in Escherichia coli

Bhaskarla, Chetana; Das, Mrinmoy; Verma, Taru; Kumar, Anujith; Mahadevan, S.; Nandi, Dipankar

doi:10.1099/mic.0.000271

Cited by 38 publications

(49 citation statements)

References 47 publications

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“…MarRAB has homologs throughout the bacteria and archaea, including many drug-resistant clinical isolates (46). In E. coli, salicylate or benzoate relieves the repression of MarA, which regulates over 60 genes involved in antibiotic resistance, such as the AcrAB-TolC MDR pump (14,47), as well as hdeAB within the slp-gad island (17). MarA downregulates the large porin OmpF, which admits nutrients and antibiotics (48).…”

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confidence: 99%

Inverted Regulation of Multidrug Efflux Pumps, Acid Resistance, and Porins in Benzoate-Evolved Escherichia coli K-12

Moore

Engmann

et al. 2019

Appl Environ Microbiol

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Benzoic acid, a partial uncoupler of the proton motive force (PMF), selects for sensitivity to chloramphenicol and tetracycline during the experimental evolution of Escherichia coli K-12. Transcriptomes of E. coli isolates evolved with benzoate showed the reversal of benzoate-dependent regulation, including the downregulation of multidrug efflux pump genes, the gene for the Gad acid resistance regulon, the nitrate reductase genes narHJ, and the gene for the acid-consuming hydrogenase Hyd-3. However, the benzoate-evolved strains had increased expression of OmpF and other large-hole porins that admit fermentable substrates and antibiotics. Candidate genes identified from benzoate-evolved strains were tested for their roles in benzoate tolerance and in chloramphenicol sensitivity. Benzoate or salicylate tolerance was increased by deletion of the Gad activator ariR or of the acid fitness island from slp to the end of the gadX gene encoding Gad regulators and the multidrug pump genes mdtEF. Benzoate tolerance was also increased by deletion of multidrug component gene emrA, RpoS posttranscriptional regulator gene cspC, adenosine deaminase gene add, hydrogenase gene hyc (Hyd-3), and the RNA chaperone/DNA-binding regulator gene hfq. Chloramphenicol resistance was decreased by mutations in genes for global regulators, such as RNA polymerase alpha subunit gene rpoA, the Mar activator gene rob, and hfq. Deletion of lipopolysaccharide biosynthetic kinase gene rfaY decreased the rate of growth in chloramphenicol. Isolates from experimental evolution with benzoate had many mutations affecting aromatic biosynthesis and catabolism, such as aroF (encoding tyrosine biosynthesis) and apt (encoding adenine phosphoribosyltransferase). Overall, benzoate or salicylate exposure selects for the loss of multidrug efflux pumps and of hydrogenases that generate a futile cycle of PMF and upregulates porins that admit fermentable nutrients and antibiotics. IMPORTANCE Benzoic acid is a common food preservative, and salicylic acid (2-hydroxybenzoic acid) is the active form of aspirin. At high concentrations, benzoic acid conducts a proton across the membrane, depleting the proton motive force. In the absence of antibiotics, benzoate exposure selects against proton-driven multidrug efflux pumps and upregulates porins that admit fermentable substrates but that also allow the entry of antibiotics. Thus, evolution with benzoate and related molecules, such as salicylates, requires a trade-off for antibiotic sensitivity, a trade-off that could help define a stable gut microbiome. Benzoate and salicylate are naturally occurring plant signal molecules that may modulate the microbiomes of plants and animal digestive tracts so as to favor fermenters and exclude drug-resistant pathogens.

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confidence: 99%

Inverted Regulation of Multidrug Efflux Pumps, Acid Resistance, and Porins in Benzoate-Evolved Escherichia coli K-12

Moore

Engmann

et al. 2019

Appl Environ Microbiol

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“…A high-force-constant (∼40 Nm−1) silicon AFM probe tip (Acta; Park Systems) was used with a resonating frequency of 300 kHz. The AFM instrument (Bioengineering facility) was operated in the non-contact mode [56].…”

Section: Atomic Force Microscopy Imagingmentioning

confidence: 99%

Salmonella Typhimurium encoded cold shock protein E is essential for motility and biofilm formation

et al. 2020

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The ability of bacteria to form biofilms increases their survival under adverse environmental conditions. Biofilms have enormous medical and environmental impact; consequently, the factors that influence biofilm formation are an important area of study. In this investigation, the roles of two cold shock proteins (CSP) during biofilm formation were investigated in Salmonella Typhimurium, which is a major foodborne pathogen. Among all CSP transcripts studied, the expression of cspE (STM14_0732) was higher during biofilm growth. The cspE deletion strain (ΔcspE) did not form biofilms on a cholesterol coated glass surface; however, complementation with WT cspE, but not the F30V mutant, was able to rescue this phenotype. Transcript levels of other CSPs demonstrated up-regulation of cspA (STM14_4399) in ΔcspE. The cspA deletion strain (ΔcspA) did not affect biofilm formation; however, ΔcspEΔcspA exhibited higher biofilm formation compared to ΔcspE. Most likely, the higher cspA amounts in ΔcspE reduced biofilm formation, which was corroborated using cspA over-expression studies. Further functional studies revealed that ΔcspE and ΔcspEΔcspA exhibited slow swimming but no swarming motility. Although cspA over-expression did not affect motility, cspE complementation restored the swarming motility of ΔcspE. The transcript levels of the major genes involved in motility in ΔcspE demonstrated lower expression of the class III (fliC, motA, cheY), but not class I (flhD) or class II (fliA, fliL), flagellar regulon genes. Overall, this study has identified the interplay of two CSPs in regulating two biological processes: CspE is essential for motility in a CspA-independent manner whereas biofilm formation is CspA-dependent.

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“…Isolated single colonies of E. coli K-12 (MG 1655) were used to prepare the pre-inoculum [54]. The culture was grown in Luria Bertani (LB) medium for 8 h at 37 • C with constant shaking at 160 rpm.…”

Section: Bacterial Growth Conditions and Sample Preparationmentioning

confidence: 99%

Facile Fabrication of Multifunctional ZnO Urchins on Surfaces

Tripathy

Wąsik

Sreedharan

et al. 2018

Colloids and Interfaces

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Functional ZnO nanostructured surfaces are important in a wide range of applications. Here we report the simple fabrication of ZnO surface structures at near room temperature with morphology resembling that of sea urchins, with densely packed, µm-long, tapered nanoneedles radiating from the urchin center. The ZnO urchin structures were successfully formed on several different substrates with high surface density and coverage, including silicon (Si), glass, polydimethylsiloxane (PDMS), and copper (Cu) sheets, as well as Si seeded with ZnO nanocrystals. Time-resolved SEM revealed growth kinetics of the ZnO nanostructures on Si, capturing the emergence of "infant" urchins at the early growth stage and subsequent progressive increases in the urchin nanoneedle length and density, whilst the spiky nanoneedle morphology was retained throughout the growth. ε-Zn(OH) 2 orthorhombic crystals were also observed alongside the urchins. The crystal structures of the nanostructures at different growth times were confirmed by synchrotron X-ray diffraction measurements. On seeded Si substrates, a two-stage growth mechanism was identified, with a primary growth step of vertically aligned ZnO nanoneedle arrays preceding the secondary growth of the urchins atop the nanoneedle array. The antibacterial, anti-reflective, and wetting functionality of the ZnO urchins-with spiky nanoneedles and at high surface density-on Si substrates was demonstrated. First, bacteria colonization was found to be suppressed on the surface after 24 h incubation in gram-negative Escherichia coli (E. coli) culture, in contrast to control substrates (bare Si and Si sputtered with a 20 nm ZnO thin film). Secondly, the ZnO urchin surface, exhibiting superhydrophilic property with a water contact angle ∼ 0 • , could be rendered superhydrophobic with a simple silanization step, characterized by an apparent water contact angle θ of 159 • ± 1.4 • and contact angle hysteresis ∆θ < 7 • . The dynamic superhydrophobicity of the surface was demonstrated by the bouncing-off of a falling 10 µL water droplet, with a contact time of 15.3 milliseconds (ms), captured using a high-speed camera. Thirdly, it was shown that the presence of dense spiky ZnO nanoneedles and urchins on the seeded Si substrate exhibited a reflectance R < 1% over the wavelength range λ = 200-800 nm. The ZnO urchins with a unique morphology fabricated via a simple route at room temperature, and readily implementable on different substrates, may be further exploited for multifunctional surfaces and product formulations.

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Roles of Lon protease and its substrate MarA during sodium salicylate-mediated growth reduction and antibiotic resistance in Escherichia coli

Cited by 38 publications

References 47 publications

Inverted Regulation of Multidrug Efflux Pumps, Acid Resistance, and Porins in Benzoate-Evolved Escherichia coli K-12

Inverted Regulation of Multidrug Efflux Pumps, Acid Resistance, and Porins in Benzoate-Evolved Escherichia coli K-12

Salmonella Typhimurium encoded cold shock protein E is essential for motility and biofilm formation

Facile Fabrication of Multifunctional ZnO Urchins on Surfaces

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