Genetic determinants of heat resistance in Escherichia coli

Mercer, Ryan G.; Zheng, Jinshui; Garcia-Hernandez, Rigoberto; Ruan, Lifang; Gänzle, Michael G.; McMullen, Lynn M.

doi:10.3389/fmicb.2015.00932

Cited by 115 publications

(226 citation statements)

References 58 publications

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“…coli strains (32), was also assessed in chlorine-tolerant wastewater strains. PCRs targeting three fragments of this genomic island were performed on all 70 wastewater E.…”

Section: Methodsmentioning

confidence: 99%

Evidence of Naturalized Stress-Tolerant Strains of Escherichia coli in Municipal Wastewater Treatment Plants

Zhi

Banting

et al. 2016

Appl Environ Microbiol

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Escherichia coli has been proposed to have two habitats—the intestines of mammals/birds and the nonhost environment. Our goal was to assess whether certain strains of E. coli have evolved toward adaptation and survival in wastewater. Raw sewage samples from different treatment plants were subjected to chlorine stress, and ∼59% of the surviving E. coli strains were found to contain a genetic insertion element (IS30) located within the uspC-flhDC intergenic region. The positional location of the IS30 element was not observed across a library of 845 E. coli isolates collected from various animal hosts or within GenBank or whole-genome reference databases for human and animal E. coli isolates (n = 1,177). Phylogenetics clustered the IS30 element-containing wastewater E. coli isolates into a distinct clade, and biomarker analysis revealed that these wastewater isolates contained a single nucleotide polymorphism (SNP) biomarker pattern that was specific for wastewater. These isolates belonged to phylogroup A, possessed generalized stress response (RpoS) activity, and carried the locus of heat resistance, features likely relevant to nonhost environmental survival. Isolates were screened for 28 virulence genes but carried only the fimH marker. Our data suggest that wastewater contains a naturalized resident population of E. coli. We developed an endpoint PCR targeting the IS30 element within the uspC-flhDC intergenic region, and all raw sewage samples (n = 21) were positive for this marker. Conversely, the prevalence of this marker in E. coli-positive surface and groundwater samples was low (≤5%). This simple PCR assay may represent a convenient microbial source-tracking tool for identification of water samples affected by municipal wastewater.IMPORTANCE The results of this study demonstrate that some strains of E. coli appear to have evolved to become naturalized populations in the wastewater environment and possess a number of stress-related genetic elements likely important for survival in this nonhost environment. The presence of non-host-adapted strains in wastewater challenges our understanding of using E. coli as a microbial indicator of wastewater treatment performance, suggesting that the E. coli strains present in human and animal feces may be very different from those found in treated wastewater.

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“…coli strains (32), was also assessed in chlorine-tolerant wastewater strains. PCRs targeting three fragments of this genomic island were performed on all 70 wastewater E.…”

Section: Methodsmentioning

confidence: 99%

Evidence of Naturalized Stress-Tolerant Strains of Escherichia coli in Municipal Wastewater Treatment Plants

Zhi

Banting

et al. 2016

Appl Environ Microbiol

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“…It should be underscored, however, that in these laboratory-directed evolution experiments, evolvability is typically restricted to the available genomic repertoire, while in more natural settings, lateral gene transfer can be an important driver of adaptation. In this context, it was recently shown that the ability of extremely heat-resistant E. coli strains, which were isolated from a slaughterhouse plant using steam-based carcass decontamination, to survive exposures up to 71°C stemmed from the lateral acquisition of a genomic island termed the locus of heat resistance (27,28).…”

Section: Discussionmentioning

confidence: 99%

Stress-Induced Evolution of Heat Resistance and Resuscitation Speed in Escherichia coli O157:H7 ATCC 43888

Gayán

Cambré

Michiels

et al. 2016

Appl Environ Microbiol

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The development of resistance in foodborne pathogens to food preservation techniques is an issue of increasing concern, especially in minimally processed foods where safety relies on hurdle technology. In this context, mild heat can be used in combination with so-called nonthermal processes, such as high hydrostatic pressure (HHP), at lower individual intensities to better retain the quality of the food. However, mild stresses may increase the risk of (cross-)resistance development in the surviving population, which in turn might compromise food safety. In this investigation, we examined the evolution of Escherichia coli O157:H7 strain ATCC 43888 after recurrent exposure to progressively intensifying mild heat shocks (from 54.0°C to 60.0°C in 0.5°C increments) with intermittent resuscitation and growth of survivors. As such, mutant strains were obtained after 10 cycles of selection with ca. 10 6 -fold higher heat resistance than that for the parental strain at 58.0°C, although this resistance did not extend to temperatures exceeding 60.0°C. Moreover, these mutant strains typically displayed cross-resistance against HHP shock and displayed signs of enhanced RpoS and RpoH activity. Interestingly, additional cycles of selection maintaining the intensity of the heat shock constant (58.5°C) selected for mutant strains in which resuscitation speed, rather than resistance, appeared to be increased. Therefore, it seems that resistance and resuscitation speed are rapidly evolvable traits in E. coli ATCC 43888 that can compromise food safety. IMPORTANCEIn this investigation, we demonstrated that Escherichia coli O157:H7 ATCC 43888 rapidly acquires resistance to mild heat exposure, with this resistance yielding cross-protection to high hydrostatic pressure treatment. In addition, mutants of E. coli ATCC 43888 in which resuscitation speed, rather than resistance, appeared to be improved were selected. As such, both resistance and resuscitation speed seem to be rapidly evolvable traits that can compromise the control of foodborne pathogens in minimal processing strategies, which rely on the efficacy of combined mild preservation stresses for food safety. Minimal processing of foods is based on the combination of mild preservation methods (or hurdles) for maximizing retention of the sensorial and nutritional properties of the food while maintaining the appropriate level of food safety and shelf life (1, 2). Methods such as mild heating, acidification, and the use of natural antimicrobial compounds, high hydrostatic pressure (HHP), pulsed electric fields, ultrasound, and irradiation are some of the techniques commonly used in hurdle approaches (2-4). While the efficacy of minimal processing relies on the additive, or even synergistic, lethal or growth-inhibitory effects of such mild hurdles, the mild intensity might nevertheless pose the risk of increasing resistance to the corresponding treatments. More specifically, rare mutant strains with an increased stress resistance that can spontaneously emerge in a population ...

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“…A genomic region with a high degree of sequence similarity was recently described also in thermotolerant Klebsiella pneumoniae strains responsible for nosocomial infections due to increased resistance to disinfection protocols (Bojer et al 2010) and in several heat resistant E. coli strains isolated from beef samples (Mercer et al 2015).…”

Section: Comparison Of Thermotolerance Islands In Cronobacter Strainsmentioning

confidence: 98%

“…However, it is not known if the thermotolerance island is present in this strain. The presence of the long version of the thermotolerance island correlated with heat resistance in E. coli and complementation generating thermotolerance was achieved only if the entire genomic island was cloned into a sensitive E. coli strain and thus the thermoresistance was dependent on the entire genomic island, and not on the function of a single protein (Mercer et al 2015).…”

Section: Cloning Of the Thermotolerance Islandmentioning

confidence: 99%

Contribution of the thermotolerance genomic island to increased thermal tolerance in Cronobacter strains

Orieskova

Kajsik

Szemes

et al. 2016

Antonie van Leeuwenhoek

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Cronobacter spp. are opportunistic pathogens associated with serious infections in neonates. Increased stress tolerance, including the thermotolerance of some Cronobacter strains, can promote their survival in production facilities and thus raise the possibility of contamination of dried infant formula which has been identified as a potential source of infection. Some Cronobacter strains contain a genomic island, which might be responsible for increased thermotolerance. By analysis of Cronobacter sequenced genomes this determinant was found to be present in only 49/73 Cronobacter sakazakii strains and in 9/14 Cronobacter malonaticus strains. The island was also found in 16/17 clinical isolates originating from two hospitals. Two configurations of the locus were detected; the first one with the size of 18 kbp containing the thrB-Q genes and a shorter version (6 kbp) harbouring only the thrBCD and thrOP genes. Strains containing the thermotolerance island survived significantly better at 58°C comparing to a C. sakazakii isogenic mutant lacking the island and strains with the longer version of the island were 2-10 times more tolerant than those with the shortened sequence. The function of the genomic island was further confirmed by its cloning into a low-copy vector and transforming it into the isogenic mutant. Different levels of rpoS, encoding for stress-response sigma factor, expression were also associated with variability in strain thermotolerance.

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Genetic determinants of heat resistance in Escherichia coli

Cited by 115 publications

References 58 publications

Evidence of Naturalized Stress-Tolerant Strains of Escherichia coli in Municipal Wastewater Treatment Plants

Evidence of Naturalized Stress-Tolerant Strains of Escherichia coli in Municipal Wastewater Treatment Plants

Stress-Induced Evolution of Heat Resistance and Resuscitation Speed in Escherichia coli O157:H7 ATCC 43888

Contribution of the thermotolerance genomic island to increased thermal tolerance in Cronobacter strains

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