Genotype-by-Environment Interactions Influencing the Emergence of <i>rpoS</i> Mutations in <i>Escherichia coli</i> Populations

King, Thea; Seeto, Shona; Ferenci, Thomas

doi:10.1534/genetics.105.053892

Cited by 45 publications

(44 citation statements)

References 53 publications

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“…In particular, DPI-2 (rpoS imp ) demonstrated the highest competitive fitness. rpoS imp mutants often have an advantage over both rpoS À and rpoS þ strains in environments that may present a pH challenge (Farrell and Finkel, 2003;King et al, 2004King et al, , 2006. In this study, cells would have encountered high pH when they reached stationary phase in LB.…”

Section: Discussionmentioning

confidence: 93%

“…As the culture approaches stationary phase, s 38 increases in concentration and competes with s 70 for binding with the core polymerase (Ishihama, 2000). This leads to competing priorities for bacteria: regulation via s 38 provides protection against multiple stresses, particularly low pH (Farrell and Finkel, 2003;King et al, 2006), whereas regulation via s 70 provides improved nutrient scavenging (Notley-McRobb et al, 2002). Consequently, null or attenuation mutations of rpoS are common in laboratory conditions where improved scavenging can provide a selective advantage.…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage

2008

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Rapid evolution of microbes under laboratory conditions can lead to domestication of environmental or clinical strains. In this work, we show that domestication due to laboratory passage in rich medium is extremely rapid. Passaging of wild-type Salmonella in rich medium led to diversification of genotypes contributing to the loss of a spatial phenotype, called the rdar morphotype, within days. Gene expression analysis of the rdar regulatory network demonstrated that mutations were primarily within rpoS, indicating that the selection pressure for scavenging during stationary phase had the secondary effect of impairing this highly conserved phenotype. If stationary phase was omitted from the experiment, radiation of genotypes and loss of the rdar morphotype was also demonstrated, but due to mutations within the cellulose biosynthesis pathway and also in an unknown upstream regulator. Thus regardless of the selection pressure, rapid regulatory changes can be observed on laboratory timescales. The speed of accumulation of rpoS mutations during daily passaging could not be explained by measured fitness and mutation rates. A model of mutation accumulation suggests that to generate the observed accumulation of r 38 mutations, this locus must experience a mutation rate of approximately 10 À4 mutations/gene/generation. Sequencing and gene expression of population isolates indicated that there were a wide variety of r 38 phenotypes within each population. This suggests that the rpoS locus is highly mutable by an unknown pathway, and that these mutations accumulate rapidly under common laboratory conditions.

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Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage

2008

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“…Constant mutational selection in fluctuating environments or environments where neither of two traits is entirely beneficial can lead to the mutational reassortment of the SPANC balance. In the case of the rpoSdetermined trade-off, there is selection for intermediate settings of the SPANC balance when bacteria are evolving under nutrient limitation but moderate environmental stress (King et al, 2006). This propensity for optimizing fitness in distinct environments leads to species-wide diversity in the concentration of RpoS (and molecules that regulate RpoS) across isolates of E. coli in the same environment (Ferenci et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Phan

Ferenci

2013

The ISME Journal

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Bacterial species are internally diverse in genomic and multi-locus gene comparisons. The ecological causes of phenotypic and genotypic diversity within species are far less well understood. Here, we focus on the competitive fitness for growth on nutrients within Escherichia coli, an internally rich species. Competition experiments in nutrient-limited chemostats revealed that members of the ECOR collection exhibited a wide continuum of competitive abilities, with some fitter and some less fit than the lab strain MG1655. We observed an inverse relationship between competitiveness and the resistance of strains to detergent and antibiotic, consistent with the notion that membrane permeability and competitive fitness are linked by a trade-off between selfpreservation and nutritional competence (SPANC); high permeability has a postulated cost in antibacterial sensitivity whereas a low permeability has a cost in nutrient affinity. Isolates moved along the markedly nonlinear trade-off curve by mutational adaptation; an ECOR strain sensitive to antibacterials and a good competitor was easily converted by mutation into a mutant with higher resistance but poorer competition in the presence of low antibiotic concentrations. Conversely, a resistant ECOR strain changed into a better competitor after a short period of selection under nutrient limitation. In both directions, mutations can affect porin proteins and outer membrane permeability, as indicated by protein analysis, gene sequencing and an independent assay of outer membrane permeability. The extensive, species-wide diversity of E. coli in ecologically important traits can thus be explained as an evolutionary consequence of a SPANC trade-off driven by antagonistic pleiotropy.

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“…The balance between self-protection and nutritional capability, the SPANC balance, is frequently reset by mutation, resulting in many different combinations of stress resistance and nutritional capability in the species (King et al, 2004). Growth of bacteria on poor carbon sources or low levels of nutrients selects for reduced or abolished RpoS levels, whereas stressful environments require RpoS (King et al, 2006). Laboratory strains contain one of several different alleles of rpoS (Atlung et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Strain variation in ppGpp concentration and RpoS levels in laboratory strains of Escherichia coli K-12

Spira

Ferenci

2008

Microbiology

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Laboratory strains and natural isolates of Escherichia coli differ in their level of stress resistance due to strain variation in the level of the sigma factor s S (or RpoS), the transcriptional master controller of the general stress response. We found that the high level of RpoS in one laboratory strain (MC4100) was partially dependent on an elevated basal level of ppGpp, an alarmone responding to stress and starvation. The elevated ppGpp was caused by two mutations in spoT, a gene associated with ppGpp synthesis and degradation. The nature of the spoT allele influenced the level of ppGpp in both MC4100 and another commonly used K-12 strain, MG1655. Introduction of the spoT mutation into MG1655 also resulted in an increased level of RpoS, but the amount of RpoS was lower in MG1655 than in MC4100 with either the wild-type or mutant spoT allele. In both MC4100 and MG1655, high ppGpp concentration increased RpoS levels, which in turn reduced growth with poor carbon sources like acetate. The growth inhibition resulting from elevated ppGpp was relieved by rpoS mutations. The extent of the growth inhibition by ppGpp, as well as the magnitude of the relief by rpoS mutations, differed between MG1655 and MC4100. These results together suggest that spoT mutations represent one of several polymorphisms influencing the strain variation of RpoS levels. Stress resistance was higher in strains with the spoT mutation, which is consistent with the conclusion that microevolution affecting either or both ppGpp and RpoS can reset the balance between self-protection and nutritional capability, the SPANC balance, in individual strains of E. coli.

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Genotype-by-Environment Interactions Influencing the Emergence of rpoS Mutations in Escherichia coli Populations

Cited by 45 publications

References 53 publications

Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage

Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Strain variation in ppGpp concentration and RpoS levels in laboratory strains of Escherichia coli K-12

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