Household Clustering of Escherichia coli Sequence Type 131 Clinical and Fecal Isolates According to Whole Genome Sequence Analysis

Johnson, James R.; Davis, Gregg S.; Clabots, Connie; Johnston, Brian; Porter, Stephen; DebRoy, Chitrita; Pomputius, William F.; Ender, Peter T.; Cooperstock, Michael; Slater, Billie Savvas; Banerjee, Ritu; Miller, Sybille; Kisiela, Dagmara I.; Sokurenko, Evgeni V.; Aziz, Maliha; Price, Lance B.

doi:10.1093/ofid/ofw129

Cited by 60 publications

(58 citation statements)

References 38 publications

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“…This study has shown that in about half of such cases, this is due to the immigration and establishment of strains and not within‐host evolution. Thus, the results of this study show that despite hosts being regularly exposed to a diversity of E. coli through the food that they consume and the individuals they associate with (Blyton et al ., ; Johnson et al ., ), factors related to the host, at least in part, determine what E. coli strains succeed in establishing.…”

Section: Discussionmentioning

confidence: 99%

Within‐host evolution versus immigration as a determinant of Escherichia coli diversity in the human gastrointestinal tract

Dixit

O’Brien

Pavli

et al. 2017

Environmental Microbiology

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When a human host harbors two or more strains of Escherichia coli, the second strain is more likely to be a member of the same phylogroup rather than a different phylogroup. This outcome may be the consequence of a within host evolution event or an independent immigration/establishment event. To determine the relative importance of these two events in determining E. coli diversity in a host, a collection of multiple E. coli isolates recovered from each of 67 patients undergoing colonoscopies was used. Whole genome sequence data were available for one example of every REP-fingerprint type identified in a patient. Sequence type (ST) and single-nucleotide polymorphism (SNP) analyses revealed that 83% of strains observed in the host population were a consequence of immigration/establishment events. Restricting the analysis to hosts harboring two or more strains belonging to the same phylogroup revealed that in about half of these cases, the presence of a second strain belonging to the same phylogroup was the consequence of an independent immigration/establishment event. Thus, the results of this study show that despite hosts being exposed to a diversity of E. coli via their food, factors related to the host also determine what E. coli strains succeed in establishing.

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Section: Discussionmentioning

confidence: 99%

Within‐host evolution versus immigration as a determinant of Escherichia coli diversity in the human gastrointestinal tract

Dixit

O’Brien

Pavli

et al. 2017

Environmental Microbiology

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“…The fully assembled reference genomes for JJ1886 (NC_022648 [80]) and JJ1887 (NZ_CP014316 [81]) were aligned to each other using Progressive Mauve (82) and inspected for large-scale rearrangements, inversions, and duplications. Candidate sequence variations were reported directly from the alignment and confirmed by mapping raw Illumina reads obtained for those genomes (11,16) to the assembled reference sequences using Bowtie 2 (83). The alignments were refined using SAMtools (84).…”

Section: Methodsmentioning

confidence: 99%

“…For SNP analysis, raw Illumina sequencing reads (16) were aligned to the reference genome (JJ1886 or JJ1887) using the BWA-MEM algorithm (85). The alignments were refined with SAMtools (84), and variants were called using BCFtools (http://www.htslib.org).…”

Section: Methodsmentioning

confidence: 99%

“…Of these SNPs, one resulted in a premature stop codon, five were nonsynonymous (i.e., amino acid replacement) mutations, and two were synonymous (i.e., silent) mutations (Table 1). According to the phylogeny (16) (Fig. 1), 5 of 8 SNPs occurred in JJ1886 (the blood isolate), including a premature stop codon mutation in rpoS, nonsynonymous mutations in lacI, lrhA, and ydjF, and a synonymous mutation in ompN.…”

Section: Importancementioning

confidence: 99%

“…1). Unlike the household 1 isolates, for the household 2 isolates only draft genome sequences were available (16).…”

Section: Importancementioning

confidence: 99%

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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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The Public Health Risk of Companion Animal to Human Transmission of Antimicrobial Resistance During Different Types of Animal Infection

Pomba

Belas

Menezes

et al. 2020

Advances in Animal Health, Medicine and Production

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Household Clustering of Escherichia coli Sequence Type 131 Clinical and Fecal Isolates According to Whole Genome Sequence Analysis

Cited by 60 publications

References 38 publications

Within‐host evolution versus immigration as a determinant of Escherichia coli diversity in the human gastrointestinal tract

Within‐host evolution versus immigration as a determinant of Escherichia coli diversity in the human gastrointestinal tract

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

The Public Health Risk of Companion Animal to Human Transmission of Antimicrobial Resistance During Different Types of Animal Infection

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