Dataset Information

Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide.

ABSTRACT: Salmonella enterica serovar Typhimurium can differentiate into hyperflagellated swarmer cells on agar of an appropriate consistency (0.5 to 0.8%), allowing efficient colonization of the growth surface. Flagella are essential for this form of motility. In order to identify genes involved in swarming, we carried out extensive transposon mutagenesis of serovar Typhimurium, screening for those that had functional flagella yet were unable to swarm. A majority of these mutants were defective in lipopolysaccharide (LPS) synthesis, a large number were defective in chemotaxis, and some had defects in putative two-component signaling components. While the latter two classes were defective in swarmer cell differentiation, representative LPS mutants were not and could be rescued for swarming by external addition of a biosurfactant. A mutation in waaG (LPS core modification) secreted copious amounts of slime and showed a precocious swarming phenotype. We suggest that the O antigen improves surface "wettability" required for swarm colony expansion, that the LPS core could play a role in slime generation, and that multiple two-component systems cooperate to promote swarmer cell differentiation. The failure to identify specific swarming signals such as amino acids, pH changes, oxygen, iron starvation, increased viscosity, flagellar rotation, or autoinducers leads us to consider a model in which the external slime is itself both the signal and the milieu for swarming motility. The model explains the cell density dependence of the swarming phenomenon.

SUBMITTER: Toguchi A

PROVIDER: S-EPMC94776 | biostudies-literature | 2000 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide.

Toguchi A A Siano M M Burkart M M Harshey R M RM

Journal of bacteriology 20001101 22

Salmonella enterica serovar Typhimurium can differentiate into hyperflagellated swarmer cells on agar of an appropriate consistency (0.5 to 0.8%), allowing efficient colonization of the growth surface. Flagella are essential for this form of motility. In order to identify genes involved in swarming, we carried out extensive transposon mutagenesis of serovar Typhimurium, screening for those that had functional flagella yet were unable to swarm. A majority of these mutants were defective in lipopo ...[more]

PMID: 11053374

Similar Datasets

Project description:Motile bacteria employ one or more methods for movement, including darting, gliding, sliding, swarming, swimming, and twitching. Multidrug-resistant (MDR) Salmonella carries acquired genes that provide resistance to specific antibiotics, and the goal of our study was to determine how antibiotics influence swimming and swarming in such resistant Salmonella isolates. Differences in motility were examined for six MDR Salmonella enterica serovar Typhimurium isolates grown on swimming and swarming media containing subinhibitory concentrations of chloramphenicol, kanamycin, streptomycin, or tetracycline. Chloramphenicol and tetracycline reduced both swimming and swarming, though the effect was more pronounced for swimming than for swarming at the same antibiotic and concentration. Swimming was limited by kanamycin and streptomycin, but these antibiotics had much less influence on decreasing swarming. Interestingly, kanamycin significantly increased swarming in one of the isolates. Removal of the aphA1 kanamycin resistance gene and complementation with either the aphA1 or aphA2 kanamycin resistance gene revealed that aphA1, along with an unidentified Salmonella genetic factor, was required for the kanamycin-enhanced swarming phenotype. Screening of 25 additional kanamycin-resistant isolates identified two that also had significantly increased swarming motility in the presence of kanamycin. This study demonstrated that many variables influence how antibiotics impact swimming and swarming motility in MDR S. Typhimurium, including antibiotic type, antibiotic concentration, antibiotic resistance gene, and isolate-specific factors. Identifying these isolate-specific factors and how they interact will be important to better understand how antibiotics influence MDR Salmonella motility. IMPORTANCESalmonella is one of the most common causes of bacterial foodborne infections in the United States, and the Centers for Disease Control consider multidrug-resistant (MDR) Salmonella a "Serious Threat Level pathogen." Because MDR Salmonella can lead to more severe disease in patients than that caused by antibiotic-sensitive strains, it is important to identify the role that antibiotics may play in enhancing Salmonella virulence. The current study examined several MDR Salmonella isolates and determined the effect that various antibiotics had on Salmonella motility, an important virulence-associated factor. While most antibiotics had a neutral or negative effect on motility, we found that kanamycin actually enhanced MDR Salmonella swarming in some isolates. Subsequent experiments showed this phenotype as being dependent on a combination of several different genetic factors. Understanding the influence that antibiotics have on MDR Salmonella motility is critical to the proper selection and prudent use of antibiotics for efficacious treatment while minimizing potential collateral consequences.

Project description:Many bacteria are motile only when nutrients are scarce. In contrast, Salmonella enterica serovar Typhimurium is motile only when nutrients are plentiful, suggesting that this bacterium uses motility for purposes other than foraging, most likely for host colonization. In this study, we investigated how nutrients affect motility in S. enterica and found that they tune the fraction of motile cells. In particular, we observed coexisting populations of motile and nonmotile cells, with the distribution being determined by the concentration of nutrients in the growth medium. Interestingly, S. enterica responds not to a single nutrient but apparently to a complex mixture of them. Using a combination of experimentation and mathematical modeling, we investigated the mechanism governing this behavior and found that it results from two antagonizing regulatory proteins, FliZ and YdiV. We also found that a positive feedback loop involving the alternate sigma factor FliA is required, although its role appears solely to amplify FliZ expression. We further demonstrate that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. Together, these results uncover a new facet of the regulation of the flagellar genes in S. enterica and further demonstrate how bacteria employ phenotypic diversity as a general mechanism for adapting to change in their environment.Many bacteria employ flagella for motility. These bacteria are often not constitutively motile but become so only in response to specific environmental cues. The most common is nutrient starvation. Interestingly, in Salmonella enterica serovar Typhimurium, nutrients enhance the expression of flagella, suggesting that motility is used for purposes other than foraging. In this work, we investigated how nutrients affect motility in S. enterica and found that nutrients tune the fraction of motile cells within a population. Using both experimental and mathematical analysis, we determined the mechanism governing this tunable response. We further demonstrated that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. These results reveal a new facet of motility in S. enterica and demonstrate that nutrients determine not only where these bacteria swim but also the fraction of them that do so.

Project description:Salmonella enterica serovar Typhimurium (S Typhimurium) relies upon the inner membrane protein PbgA to enhance outer membrane (OM) integrity and promote virulence in mice. The PbgA transmembrane domain (residues 1 to 190) is essential for viability, while the periplasmic domain (residues 191 to 586) is dispensable. Residues within the basic region (residues 191 to 245) bind acidic phosphates on polar phospholipids, like for cardiolipins, and are necessary for salmonella OM integrity. S Typhimurium bacteria increase their OM cardiolipin concentrations during activation of the PhoPQ regulators. The mechanism involves PbgA's periplasmic globular region (residues 245 to 586), but the biological role of increasing cardiolipins on the surface is not understood. Nonsynonymous polymorphisms in three essential lipopolysaccharide (LPS) synthesis regulators, lapB (also known as yciM), ftsH, and lpxC, variably suppressed the defects in OM integrity, rifampin resistance, survival in macrophages, and systemic colonization of mice in the pbgAΔ191-586 mutant (in which the PbgA periplasmic domain from residues 191 to 586 is deleted). Compared to the OMs of the wild-type salmonellae, the OMs of the pbgA mutants had increased levels of lipid A-core molecules, cardiolipins, and phosphatidylethanolamines and decreased levels of specific phospholipids with cyclopropanated fatty acids. Complementation and substitution mutations in LapB and LpxC generally restored the phospholipid and LPS assembly defects for the pbgA mutants. During bacteremia, mice infected with the pbgA mutants survived and cleared the bacteria, while animals infected with wild-type salmonellae succumbed within 1 week. Remarkably, wild-type mice survived asymptomatically with pbgA-lpxC salmonellae in their livers and spleens for months, but Toll-like receptor 4-deficient animals succumbed to these infections within roughly 1 week. In summary, S Typhimurium uses PbgA to influence LPS assembly during stress in order to survive, adapt, and proliferate within the host environment.

Dataset Information

Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide.

Publications

Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets