Polymorphism and selection of rpoS in pathogenic Escherichia coli

Dong, Tao; Chiang, Sarah M.; Joyce, Charlie; Yu, Rong; Schellhorn, Herb E.

doi:10.1186/1471-2180-9-118

Cited by 47 publications

(74 citation statements)

References 68 publications

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“…Of these 15 substrates inducing responses measured by the Biolog assay, the increased responses with L-serine and L-threonine correspond well with the increase in expression of tdcCA, genes involved in both L-threonine and L-serine uptake. Increased utilization of succinic acid (succinate) by RM6069 and RM9998 also is consistent with the SPANC hypothesis and the ability to select rpoS mutants on succinate minimal medium (14).…”

Section: Resultssupporting

confidence: 69%

“…A relevant part of the hypothesis specifically suggests that competition between S and 70 defines the gene expression and phenotypes exhibited by the bacteria (22). In fact, rpoS mutants have been selected for by growth on nonpreferred carbon sources (14). Here, we demonstrated that the clinical and spinach isolates with mutations within rpoS and/or with decreased levels of S exhibited decreased expression of stress-related genes (see Table S1 in the supplemental material) and lower resistance to acid, high-salt conditions, and oxidation (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…The rpoS gene encodes the stationary-phase sigma factor, S , a global regulator that coordinates the expression of a large network of genes upon cells entering stationary phase or during exposure of cells to stresses such as acidity or high osmolarity (43). The appearance of rpoS mutants seems to be driven by the increased ability of such mutants to scavenge for scarce nutrients (22,33); for example, rpoS mutants have been selected for by growth on nonpreferred carbon sources (14). Thus, rpoS mutants and strains with reduced S levels sacrifice their ability to adapt to certain stresses in favor of nutritional scavenging in some environments.…”

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confidence: 99%

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Distinct Transcriptional Profiles and Phenotypes Exhibited by Escherichia coli O157:H7 Isolates Related to the 2006 Spinach-Associated Outbreak

Parker

Kyle

Huynh

et al. 2012

Appl Environ Microbiol

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In 2006, a large outbreak of Escherichia coli O157:H7 was linked to the consumption of ready-to-eat bagged baby spinach in the United States. The likely sources of preharvest spinach contamination were soil and water that became contaminated via cattle or feral pigs in the proximity of the spinach fields. In this study, we compared the transcriptional profiles of 12 E. coli O157:H7 isolates that possess the same two-enzyme pulsed-field gel electrophoresis (PFGE) profile and are related temporally or geographically to the above outbreak. These E. coli O157:H7 isolates included three clinical isolates, five isolates from separate bags of spinach, and single isolates from pasture soil, river water, cow feces, and a feral pig. The three clinical isolates and two spinach bag isolates grown in cultures to stationary phase showed decreased expression of many S -regulated genes, including gadA, osmE, osmY, and katE, compared with the soil, water, cow, feral pig, and the other three spinach bag isolates. The decreased expression of these S -regulated genes was correlated with the decreased resistance of the isolates to acid stress, osmotic stress, and oxidative stress but increases in scavenging ability. We also observed that intraisolate variability was much more pronounced among the clinical and spinach isolates than among the environmental isolates. Together, the transcriptional and phenotypic differences of the spinach outbreak isolates of E. coli O157:H7 support the hypothesis that some variants within the spinach bag retained characteristics of the preharvest isolates, whereas other variants with altered gene expression and phenotypes infected the human host.

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Section: Resultssupporting

confidence: 69%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Distinct Transcriptional Profiles and Phenotypes Exhibited by Escherichia coli O157:H7 Isolates Related to the 2006 Spinach-Associated Outbreak

Parker

Kyle

Huynh

et al. 2012

Appl Environ Microbiol

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“…Adaptive mutations within the rpoS gene are selected in laboratory and pathogenic E. coli strains in nutrient-poor conditions or during growth on nonpreferred carbon sources (13,17,61,84). Because E. coli can be found in a wide range of environments (10,34,56), including putative poor carbon environments, we postulated that RpoS mutants are present, and may be selected, in environmental E. coli populations.…”

mentioning

confidence: 99%

Phenotypic Diversity Caused by Differential RpoS Activity among Environmental Escherichia coli Isolates

Chiang

Dong

Edge

et al. 2011

Appl Environ Microbiol

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Enteric bacteria deposited into the environment by animal hosts are subject to diverse selective pressures. These pressures may act on phenotypic differences in bacterial populations and select adaptive mutations for survival in stress. As a model to study phenotypic diversity in environmental bacteria, we examined mutations of the stress response sigma factor, RpoS, in environmental Escherichia coli isolates. A total of 2,040 isolates from urban beaches and nearby fecal pollution sources on Lake Ontario (Canada) were screened for RpoS function by examining growth on succinate and catalase activity, two RpoS-dependent phenotypes. The rpoS sequence was determined for 45 isolates, including all candidate RpoS mutants, and of these, six isolates were confirmed as mutants with the complete loss of RpoS function. Similarly to laboratory strains, the RpoS expression of these environmental isolates was stationary phase dependent. However, the expression of RpoS regulon members KatE and AppA had differing levels of expression in several environmental isolates compared to those in laboratory strains. Furthermore, after plating rpoS ؉ isolates on succinate, RpoS mutants could be readily selected from environmental E. coli. Naturally isolated and succinate-selected RpoS mutants had lower generation times on poor carbon sources and lower stress resistance than their rpoS ؉ isogenic parental strains. These results show that RpoS mutants are present in the environment (with a frequency of 0.003 among isolates) and that, similarly to laboratory and pathogenic strains, growth on poor carbon sources selects for rpoS mutations in environmental E. coli. RpoS selection may be an important determinant of phenotypic diversification and, hence, the survival of E. coli in the environment.

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“…A similar role was proposed also for natural RpoS-inactivating mutations (50). However, in the in-host environment, stress and nutritional competition appear to be equally important, in that different types of mutations, i.e., loss-of-function mutations and those affecting the expression level of RpoS, are selected (51)(52)(53). Interestingly, virulence analysis of different clonally related E. coli isolates from the same patient with distinct RpoS expression levels showed that a lower level of RpoS was strongly associated with better growth in vitro and greater virulence in the murine septicemia model (51).…”

Section: Discussionmentioning

confidence: 99%

Inactivation of Transcriptional Regulators during Within-Household Evolution of Escherichia coli

et al. 2017

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We analyzed the within-household evolution of two household-associated Escherichia coli strains from pandemic clonal group ST131-H30, using isolates recovered from five individuals within two families, each of which had a distinct strain. Family 1's strain was represented by a urine isolate from the index patient (older sister) with recurrent cystitis and a blood isolate from her younger sister with fatal urosepsis. Family 2's strain was represented by a urine isolate from the index patient (father) with pyelonephritis and renal abscesses, blood and kidney drainage isolates from the daughter with emphysematous pyelonephritis, and urine and fecal isolates from the mother with cystitis. Collectively, the several variants of each family's strain had accumulated a total of 8 (family 1) and 39 (family 2) point mutations; no two isolates were identical. Of the 47 total mutations, 36 resulted in amino acid changes or truncation of coded proteins. Fourteen such mutations (39%) targeted genes encoding transcriptional regulators, and 9 (25%) involved DNA-binding transcription factors (TFs), which significantly exceeded the relative contribution of TF genes to the isolates' genomes (ϳ6%). At least one-half of the transcriptional regulator mutations were inactivating, based on phenotypic and/or transcriptional analysis. In particular, inactivating mutations in the global regulator LrhA (repressor of type 1 fimbriae and flagella) occurred in the blood isolates from both households and increased the virulence of E. coli strains in a murine sepsis model. The results indicate that E. coli undergoes adaptive evolution between and/or within hosts, generating subpopulations with distinctive phenotypes and virulence potential.IMPORTANCE The clonal evolution of bacterial strains associated with interhost transmission is poorly understood. We characterized the genome sequences of clonal descendants of two Escherichia coli strains, recovered at different time points from multiple individuals within two households who had different types of urinary tract infection. We found evidence that the E. coli strains underwent extensive mutational diversification between and within these individuals, driven disproportionately by inactivation of transcriptional regulators. In urosepsis isolates, the mutations observed in the global regulator LrhA increased bacterial virulence in a murine sepsis model. Our findings help in understanding the adaptive dynamics and strategies of E. coli during short-term natural evolution.

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Polymorphism and selection of rpoS in pathogenic Escherichia coli

Cited by 47 publications

References 68 publications

Distinct Transcriptional Profiles and Phenotypes Exhibited by Escherichia coli O157:H7 Isolates Related to the 2006 Spinach-Associated Outbreak

Distinct Transcriptional Profiles and Phenotypes Exhibited by Escherichia coli O157:H7 Isolates Related to the 2006 Spinach-Associated Outbreak

Phenotypic Diversity Caused by Differential RpoS Activity among Environmental Escherichia coli Isolates

Inactivation of Transcriptional Regulators during Within-Household Evolution of Escherichia coli

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