Only time will tell: lipopolysaccharide glycoform and biofilm-formation kinetics in Salmonella species and Escherichia coli

Abstract

In Gram-negative bacteria, LPS (lipopolysaccharide) has been thoroughly characterized and has been shown to play a major role in pathogenesis and bacterial defense. In Salmonella and Escherichia coli, LPS also influences biofilm development. However, the overall role of LPS glycoform in biofilm formation has not been conclusively settled, as there is a lack of consensus on the topic. Some studies show that LPS mutants produce less biofilm biomass than the wild-type strains, while others show that they produce more. This review summarizes current knowledge of LPS biosynthesis and explores the impact of defective steps on biofilm-related characteristics, such as motility, adhesion, auto-aggregation, and biomass production in Salmonella and E. coli. Overall, motility tends to decrease, while adhesion and auto-aggregation phenotypes tend to increase in most LPS-mutant strains. Interestingly, biofilm biomass of various LPS mutants revealed a clear pattern dependent on biofilm maturation time. Incubation times of less than 24 h resulted in a biofilm-defective phenotype compared to the wild-type, while incubation exceeding 24 h led to significantly higher levels of biofilm production. This explains conflicting results found in reports describing the same LPS mutations. It is therefore critical to consider the effect of biofilm maturation time to ascertain the effects of LPS glycoform on biofilm phenotype. Underlying reasons for such changes in biofilm kinetics may include changes in signalling systems affecting biofilm maturation and composition, and dynamic LPS modifications. A better understanding of the role of LPS in the evolution and modification of biofilms is crucial for developing strategies to disperse biofilms.

Keywords: Escherichia coli; LPS; Salmonella; biofilms; glycoform.

Fig 1

Schematic representation of the Gram-negative outer membrane, with LPS located at the cell surface.

Fig 2

(A) Overview of LPS lipid A and inner-core biosynthesis in S. Typhimurium and E. coli. BHM, β-hydroxymyristate; FA, fatty acid; Glc, glucose; Hep, heptose; P, phosphate. (B) Overview of lipid A-core modifications. Ara4N, 4-amino-4-deoxy-L-arabinose; pEtN, phosphoethanolamine. *Not found in E. coli.

Fig 3

Overview of LPS outer-core biosynthesis in S. Typhimurium and E. coli K-12. Glc, glucose; Gal, galactose; GlcNAc, N-acetylglucosamine; Hep, heptose.

Fig 4

Schematic representation of O-antigen translocation and polymerization pathways. Adapted from reference (23). [O], repeating unit of the O-antigen chain; S, sugar; NDP, nucleoside diphosphate; NMP, nucleoside monophosphate.

Fig 5

Schematic representation of uncapped S. Typhimurium LPS glycoform resulting from deletions of waaL, waaK, waaJ, waaI, waaG, waaY, waaQ, waaP, waaF, and waaC, respectively, and gene-cluster diagram of the waa locus in Salmonella sp. and E. coli for schematic representation of uncapped E. coli LPS glycoforms, see reference (59).