Membrane-derived oligosaccharides (MDOs) are essential for sodium dodecyl sulfate resistance in<i>Escherichia coli</i>

Rajagopal, Soumitra; Eis, Nicole; Bhattacharya, Monika; Nickerson, Kenneth W.

doi:10.1016/s0378-1097(03)00323-9

Cited by 23 publications

(14 citation statements)

References 17 publications

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“…Most abundant bile salts in humans are cholate and deoxycholate (DOC). Due to OPGs prime location in the periplasm, it was hypothesized that anionic charges on OPGs may act as repellent and fend off anionic detergents and could be very important during pathogenesis (Rajagopal et al 2003). Salmonella opgB and opgC mutants did not exhibit DOC sensitivity as it has been reported in previous bilesensitive mutants (Ramos-Morales et al 2003;Crawford et al 2008).…”

Section: Resultsmentioning

confidence: 91%

Role of anionic charges of osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium SL1344 in mice virulence

et al. 2012

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opgB gene of Salmonella enterica serovar Typhimurium was identified earlier in a genome-wide screen for mice virulence (Valentine et al. in Infect Immun 66:3378-3383, 1998). Although mutation in opgB resulted in avirulent Salmonella strain, how this gene contributes to pathogenesis remains unclear. Based on DNA homology, opgB is predicted to be responsible for adding phosphoglycerate residues to osmoregulated periplasmic glucans (OPGs) giving them anionic characteristics. In Escherichia coli, yet another gene, opgC, is also reported to contribute to anionic characteristics of OPGs by adding succinic acid residues. We constructed opgB, opgC, and opgBC double mutants of S. enterica serovar Typhimurium strain SL1344. As predicted opgBC mutant synthesized neutral OPGs that were devoid of any anionic substituents. However, opgB, opgC, and opgBC mutations had no significant impact on mice virulence as well as on competitive organ colonization. In low osmotic conditions, opgB, opgC, and opgBC mutants exhibited delay in growth initiation in the presence of sodium deoxycholate. Anionic substituents of OPGs from Salmonella although appear to be needed to overcome resistance of deoxycholate in hypoosmotic growth media, no evidence was found for their role in mice virulence.

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Section: Resultsmentioning

confidence: 91%

Role of anionic charges of osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium SL1344 in mice virulence

et al. 2012

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“…The loss of OPG synthesis has been implicated in a range of abnormal phenotypes including deficiencies in: envelope stability, flagellar synthesis and motility, phage infectivity, biofilm formation, and pathogenicity [21], [22], [23], [24], [25], [26], [27], [28], [29]. While some of these phenotypes can be attributed to an altered cell envelope, the majority are tied to aberrant activation of the Rcs phosphorelay [22], [30], [31].…”

Section: Resultsmentioning

confidence: 99%

A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism

et al. 2013

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Growth rate and nutrient availability are the primary determinants of size in single-celled organisms: rapidly growing Escherichia coli cells are more than twice as large as their slow growing counterparts. Here we report the identification of the glucosyltransferase OpgH as a nutrient-dependent regulator of E. coli cell size. During growth under nutrient-rich conditions, OpgH localizes to the nascent septal site, where it antagonizes assembly of the tubulin-like cell division protein FtsZ, delaying division and increasing cell size. Biochemical analysis is consistent with OpgH sequestering FtsZ from growing polymers. OpgH is functionally analogous to UgtP, a Bacillus subtilis glucosyltransferase that inhibits cell division in a growth rate-dependent fashion. In a striking example of convergent evolution, OpgH and UgtP share no homology, have distinct enzymatic activities, and appear to inhibit FtsZ assembly through different mechanisms. Comparative analysis of E. coli and B. subtilis reveals conserved aspects of growth rate regulation and cell size control that are likely to be broadly applicable. These include the conservation of uridine diphosphate glucose as a proxy for nutrient status and the use of moonlighting enzymes to couple growth rate-dependent phenomena to central metabolism.

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“…Gene deletions causing SDS and SDS-EDTA sensitivity in E. coli have previously been investigated in a high-throughput study (56); however, the study examined colony size on plates and so did not differentiate between different growth states. Several studies examining the SDS resistance of Enterobacteriaceae have touched on the SDS resistance of E. coli (57)(58)(59)(60)(61). However, the studies that examined growth phase-dependent effects were conducted in a W3110 background (58,59), which has mutations in several stress response pathways, including the Rcs pathway, and depending on the source may lack functional RpoS and/or RpoF (62,63).…”

Section: Discussionmentioning

confidence: 99%

Novel RpoS-Dependent Mechanisms Strengthen the Envelope Permeability Barrier during Stationary Phase

2017

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Gram-negative bacteria have effective methods of excluding toxic compounds, including a largely impermeable outer membrane (OM) and a range of efflux pumps. Furthermore, when cells become nutrient limited, RpoS enacts a global expression change providing cross-protection against many stresses. Here, we utilized sensitivity to an anionic detergent (sodium dodecyl sulfate [SDS]) to probe changes occurring to the cell's permeability barrier during nutrient limitation. Escherichia coli is resistant to SDS whether cells are actively growing, carbon limited, or nitrogen limited. In actively growing cells, this resistance depends on the AcrAB-TolC efflux pump; however, this pump is not necessary for protection under either carbon-limiting or nitrogen-limiting conditions, suggesting an alternative mechanism(s) of SDS resistance. In carbon-limited cells, RpoS-dependent pathways lessen the permeability of the OM, preventing the necessity for efflux. In nitrogen-limited but not carbon-limited cells, the loss of rpoS can be completely compensated for by the AcrAB-TolC efflux pump. We suggest that this difference simply reflects the fact that nitrogen-limited cells have access to a metabolizable energy (carbon) source that can efficiently power the efflux pump. Using a transposon mutant pool sequencing (Tn-Seq) approach, we identified three genes, sanA, dacA, and yhdP, that are necessary for RpoS-dependent SDS resistance in carbon-limited stationary phase. Using genetic analysis, we determined that these genes are involved in two different envelope-strengthening pathways. These genes have not previously been implicated in stationary-phase stress responses. A third novel RpoS-dependent pathway appears to strengthen the cell's permeability barrier in nitrogen-limited cells. Thus, though cells remain phenotypically SDS resistant, SDS resistance mechanisms differ significantly between growth states. IMPORTANCE Gram-negative bacteria are intrinsically resistant to detergents and many antibiotics due to synergistic activities of a strong outer membrane (OM) permeability barrier and efflux pumps that capture and expel toxic molecules eluding the barrier. When the bacteria are depleted of an essential nutrient, a program of gene expression providing cross-protection against many stresses is induced. Whether this program alters the OM to further strengthen the barrier is unknown. Here, we identify novel pathways dependent on the master regulator of stationary phase that further strengthen the OM permeability barrier during nutrient limitation, circumventing the need for efflux pumps. Decreased permeability of nutrient-limited cells to toxic compounds has important implications for designing new antibiotics capable of targeting Gram-negative bacteria that may be in a growth-limited state.KEYWORDS Escherichia coli, RpoS, efflux pumps, outer membrane, permeability, stationary phase

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Membrane-derived oligosaccharides (MDOs) are essential for sodium dodecyl sulfate resistance inEscherichia coli

Cited by 23 publications

References 17 publications

Role of anionic charges of osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium SL1344 in mice virulence

Role of anionic charges of osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium SL1344 in mice virulence

A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism

Novel RpoS-Dependent Mechanisms Strengthen the Envelope Permeability Barrier during Stationary Phase

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