rpoS Mutations and Loss of General Stress Resistance in Escherichia coli Populations as a Consequence of Conflict between Competing Stress Responses

Abstract

The general stress resistance of Escherichia coli is controlled by the RpoS sigma factor ( S ), but mutations in rpoS are surprisingly common in natural and laboratory populations. Evidence for the selective advantage of losing rpoS was obtained from experiments with nutrient-limited bacteria at different growth rates. Wild-type bacteria were rapidly displaced by rpoS mutants in both glucose-and nitrogen-limited chemostat populations. Nutrient limitation led to selection and sweeps of rpoS null mutations and loss of general stress resistance. The rate of takeover by rpoS mutants was most rapid (within 10 generations of culture) in slower-growing populations that initially express higher S levels. Competition for core RNA polymerase is the likeliest explanation for reduced expression from distinct promoters dependent on 70 and involved in the hunger response to nutrient limitation. Indeed, the mutation of rpoS led to significantly higher expression of genes contributing to the high-affinity glucose scavenging system required for the hunger response. Hence, rpoS polymorphism in E. coli populations may be viewed as the result of competition between the hunger response, which requires sigma factors other than S for expression, and the maintenance of the ability to withstand external stresses. The extent of external stress significantly influences the spread of rpoS mutations. When acid stress was simultaneously applied to glucose-limited cultures, both the phenotype and frequency of rpoS mutations were attenuated in line with the level of stress. The conflict between the hunger response and maintenance of stress resistance is a potential weakness in bacterial regulation.

Gene expression analysis of E. coli strains provides insights into the role of gene regulation in diversification

“…This trade-off was also proposed as an explanation for the high polymorphism in the rpoS gene, where specifically enteric strains have attenuated phenotypes or are completely lacking a functional gene (Ferenci, 2003). Rapid displacement of wild-type strains by strains exhibiting weaker stress responses (for example, rpoS mutants) is also commonly observed in the laboratory (Notley-McRobb et al, 2002). In general, while MG1655 displayed unique features that might be specifically associated with its primary habitat (the laboratory), such as high expression of flagellum-associated genes, the strain consistently clustered together with the commensal and displayed an overall similar strategy validating the human gut as its origin.…”

Diversification Rates Increase With Population Size and Resource Concentration in an Unstructured Habitat

“…RpoS activity is a trait that comprises a critical component of a cell's complex fitness response to stressful environments (Hengge-Aronis 2000; Notley-McRobb et al 2002;Farrell and Finkel 2003). As a measure of phenotypic, rather than genotypic, diversity, it reflects traits that more directly influence interactions and responses to abiotic factors.…”

Role of the Escherichia coli nitrate transport protein, NarU, in survival during severe nutrient starvation and slow growth

“…Prolonged growth in a chemostat favours strain selection, even during the period required for a new steady state to be achieved (Chao & Cox, 1983;Ferenci, 1999;Notley-McRobb et al, 2002). It was essential, therefore, to establish that the apparent selective advantage of strains expressing either narK or narU was due to adaptation rather than to mutant selection during the experiment.…”