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Domain 8:

Pathogenesis

Molecular Epidemiology of Extraintestinal Pathogenic

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  • Authors: James R. Johnson1, and Thomas A. Russo3
  • Editor: Michael S. Donnenberg4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: VA Medical Center, Minneapolis, MN 55417; 2: Department of Medicine, University of Minnesota, Minneapolis, MN 55455; 3: VA Western New York Healthcare System, Department of Medicine, Department of Microbiology and Immunology, Witebsky Center for Microbial Pathogenesis and Immunology, University of Buffalo, Buffalo, NY 14214; 4: Virginia Commonwealth University School of Medicine, Richmond, VA
  • Received 15 August 2017 Accepted 06 February 2018 Published 17 April 2018
  • Address correspondence to James R. Johnson, [email protected]
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  • Abstract:

    Extraintestinal pathogenic (ExPEC) are important pathogens in humans and certain animals. Molecular epidemiological analyses of ExPEC are based on structured observations of strains as they occur in the wild. By assessing real-world phenomena as they occur in authentic contexts and hosts, they provide an important complement to experimental assessment. Fundamental to the success of molecular epidemiological studies are the careful selection of subjects and the use of appropriate typing methods and statistical analysis. To date, molecular epidemiological studies have yielded numerous important insights into putative virulence factors, host-pathogen relationships, phylogenetic background, reservoirs, antimicrobial-resistant strains, clinical diagnostics, and transmission pathways of ExPEC, and have delineated areas in which further study is needed. The rapid pace of discovery of new putative virulence factors and the increasing awareness of the importance of virulence factor regulation, expression, and molecular variation should stimulate many future molecular epidemiological investigations. The growing sophistication and availability of molecular typing methodologies, and of the new computational and statistical approaches that are being developed to address the huge amounts of data that whole genome sequencing generates, provide improved tools for such studies and allow new questions to be addressed.

  • Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017

Article Version

This article is an updated version of the following content:

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0004-2017
2018-04-17
2018-11-15

Abstract:

Extraintestinal pathogenic (ExPEC) are important pathogens in humans and certain animals. Molecular epidemiological analyses of ExPEC are based on structured observations of strains as they occur in the wild. By assessing real-world phenomena as they occur in authentic contexts and hosts, they provide an important complement to experimental assessment. Fundamental to the success of molecular epidemiological studies are the careful selection of subjects and the use of appropriate typing methods and statistical analysis. To date, molecular epidemiological studies have yielded numerous important insights into putative virulence factors, host-pathogen relationships, phylogenetic background, reservoirs, antimicrobial-resistant strains, clinical diagnostics, and transmission pathways of ExPEC, and have delineated areas in which further study is needed. The rapid pace of discovery of new putative virulence factors and the increasing awareness of the importance of virulence factor regulation, expression, and molecular variation should stimulate many future molecular epidemiological investigations. The growing sophistication and availability of molecular typing methodologies, and of the new computational and statistical approaches that are being developed to address the huge amounts of data that whole genome sequencing generates, provide improved tools for such studies and allow new questions to be addressed.

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Figures

Image of Figure 1
Figure 1

Open boxes represent genes within the operon (including , structural subunit; , usher; , minor tip pilins; and , adhesin). Forward and reverse primers (right- and left-pointing black triangles, respectively, above and below the operon) are used in combinations as shown to yield the indicated PCR products (thin rectangles, below operon). Heavily striped rectangles, and allele PCR products. Solid black rectangles, gene PCR products. Finely striped rectangles, long PCR operon fragments (as generated using either flanking or internal allele-specific reverse primers, as illustrated for allele I-I′). Different and variants are associated with specific lineages, hosts, and clinical syndromes. Intraoperonic deletions that yield a null phenotype (which may be associated with compromised or asymptomatic hosts) can be detected as a truncated long-PCR product. Reprinted from reference 42 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 2

Profiles are diverse, despite all isolates deriving from the same ST, which reflects the superior resolving power of PFGE over MLST. Isolates from a given household cluster together, consistent with intrahousehold strain sharing. Scale is % profile similarity. All isolates were fluoroquinolone-resistant. H30, clonal subset within the ST131-30 clade (R1 = 30R1, Rx = 30Rx). Abbreviations: ESBL, extended-spectrum β-lactamase production; HH, household; ID, identifier; PFGE, pulsotype. Reprinted from reference 63 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 3

RAPD profiles generated by using primer 1247 ( 12 ) show O18:K1:H7 strains NU14 (cystitis: lane 3) and RS218 (neonatal meningitis: lane 4) to be indistinguishable from one another, but distinct from strain 536 (O6:K15:H31, pyelonephritis: lane 2), illustrating both the broad syndrome capability of certain ExPEC lineages and the clonal diversity of urinary tract infection-causing ExPEC strains. M (lanes 1 and 5), 100-bp marker. Reprinted from reference 160 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 4

Genomic profiles (shown in computer reconstruction), as generated for each isolate by using RAPD primers 1247, 1254, 1281, and 1283, were concatenated for cluster analysis. Pyelonephritis isolates ( = 10; “Py” strain designations) are labeled in bold if from clonal group A (CGA) ( = 5) and in lightface italic if non-CGA ( = 5). CGA isolates (bold) are bracketed and labeled as to syndrome (CY, cystitis; PY, pyelonephritis) and serogroup (O11/O17/O77) (right), with the corresponding cluster shown in bold (left). The two O15:K52:H1 control strains are bracketed and labeled by serotype. Reference strains from the Reference (ECOR) collection (bold) are identified as to phylogenetic group (right). The depth of the molecular weight ladder cluster (brackets; MW) reflects the intrinsic variability inherent in gel electrophoresis and image analysis, independent of amplification. The CGA isolates cluster together irrespective of clinical syndrome (pyelonephritis, cystitis) and geography (UCB: Berkeley, California; UMN: Minneapolis, MN; Py: multiple centers around the U.S.). Reprinted from reference 248 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 5

Meta-data include allelic variants of (extended-spectrum beta-lactamase gene) and (type-1 fimbriae adhesin gene), plus mutations in the quinolone resistance-determining region (QRDR) of (WT, wild-type). Brackets identify defined ST131 clonal subsets. Branch tips are colored by geographic region, per the key. , plasmid transformant generated for strain; , cases with putative deletions in the assembled gene. Geographic clustering is evident, some of it linked with specific accessory gene variants; e.g., within the C1/H30R clonal subset, the Southeast Asian isolates (green) are largely confined to a specific clade that consists of two subclades, one characterized by and the other by . Reprinted from reference 36 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 6

Dendrogram at left depicts phylogenetic relationships for the 72 members of the Reference (ECOR) collection, as inferred based on multilocus enzyme electrophoresis ( 67 ). The four traditional major phylogenetic groups, i.e., A, B1, B2, and D (now split into groups D and F). The nonaligned (“non”) strains (now called group E) are bracketed and labeled. Bullets at right indicate presence of putative virulence genes (, P fimbriae; , group II capsule synthesis; , S and F1C fimbriae; , aerobactin system; , serum resistance; and , type 1 fimbriae). Horizontal bars at right indicate the 10 ECOR strains isolated from humans with symptomatic UTI. The remaining strains, except for one asymptomatic bacteriuria isolate, are fecal isolates from healthy human or animal hosts. Note the concentration of (chromosomal) ExPEC-defining virulence genes , , and within phylogenetic groups B2 and D, but their occasional joint appearance also in distant lineages, consistent with coordinate horizontal transfer, giving rise to ExPEC strains in historically non-ExPEC lineages. The more scattered phylogenetic distribution of (ExPEC-defining) and is consistent with these two genes’ typically plasmid location, although also can be chromosomal. is nearly universally prevalent, consistent with its presence in other species of , presumably reflecting an origin in a shared enterobacterial ancestor. Note the concentration of UTI isolates within phylogenetic groups B2 and D and the concentration of virulence genes among UTI isolates. Note also the appreciable minority of fecal isolates with multiple virulence genes, reflecting a fecal reservoir of ExPEC. Reprinted from reference 67 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 7

Pathogenicity islands (PAIs) are indicated according to their chromosomal insertion sites next to tRNA-encoding genes. Contents, by PAI, include: PAI I (-hemolysin, F17-like fimbriae, CS12-like fimbriae); PAI II (-hemolysin, P fimbriae with III); PAI III (S fimbriae, siderophore system, Tsh-like hemoglobin protease); PAI IV (yersiniabactin system). Many additional smaller DNA insertions compared to K-12 are present (not shown). Linkage of virulence genes in PAIs contributes to statistical associations between different virulence genes and between specific virulence genes and the lineages within which the corresponding PAIs tend to occur. Reprinted from reference 121 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 8

Known or putative open reading frames (ORFs) are grouped according to the following characteristics: blue, functional, known ORFs; green, truncated ORFs with a start codon and a stop codon; gray, as-yet-unidentified ORFs without homologues on the DNA level. Nonfunctional ORFs (e.g., due to internal stop codons or frameshifts) are indicated by hatched symbols. ORF numbers are indicated below the corresponding ORF symbols. Functional or truncated tRNA-encoding genes are marked in red. Direct repeat (DR) structures flanking PAIs are indicated. Thick black lines below the PAIs represent regions that were detected by PCR. Several PAI-specific PCRs were grouped into PAI regions. The molecular epidemiology of novel ORFs that are discovered through sequence analysis of PAIs can be investigated in subsequent studies. Reprinted from reference 121 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 9

binding of isogenic recombinant strains expressing the Ala-62 or Ser-62 FimH variants (from strains NU14 and 536, respectively) to (A) a trimannose substrate (bovine RNAse B), (B) human collagen type IV, and (C) a monomannose substrate (yeast mannan). Both variants bind equally well to trimannose, but the Ala-62 variant exhibits stronger type IV collagen and monomannose binding than does the Ser-62 variant. (Commensal-associated FimH variants exhibit equally strong trimannose binding but minimal binding to type IV collagen or monomannose [not shown].) Open columns, bacteria incubated without -methyl mannoside (mM); solid columns, bacteria incubated with 50 mM mM. Data are mean + SEM ( = 4) of number of bacteria bound per well. Molecular epidemiological studies can be used to elucidate the likely clinical relevance of such genetic and phenotypic variation within different virulence factors. Adapted from reference 160 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Image of Figure 10
Figure 10

(Top panel) PFGE profiles. Lane numbers are shown below gel images. Lanes 1 through 10, profiles of nine of the unique strains, with strain designations shown above gel lanes, plus subtype 1″) (lane 9). Lanes 11 through 16, profiles of independent isolates of strain 1, as recovered from various anatomical sites from the woman (lanes 11–13), man (lanes 14 and 15), and cat (lane 16). (Bottom panel) Distribution of 14 unique strains over time (week of sampling shown below grid), as recovered from various anatomical sites from the three household members. NG, no growth; •, no sample. Strains isolated more than once appear in colored boxes, with a unique color for each strain. Strains isolated only once appear in colorless boxes. Week 12, which coincided with symptoms of acute urinary tract infection (UTI) in the woman, yielded strain 1 from the woman’s urine specimen (boldface box). There is no strain 7. Strain 1, the woman’s UTI strain, was the most extensively shared and persistent strain, and had the most virulence genes of the 14 strains. Reprinted from reference 242 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Figure 11

The tree was based on 1000 bootstrapped maximum likelihood trees, retaining only those nodes that appeared in >70% of trees, and was rooted with strain CD306. Branch lengths are meaningless. Household isolates (as in Fig. 2 ) are color-coded by household ( 1 6 ); comparison isolates are shown in black. For the household isolates: boldface indicates clinical isolates; regular font indicates fecal isolates; underlining indicates fecal isolates from a clinical isolate’s source host; and asterisks indicate the 6 household isolates that were included in Price et al ( 11 ), i.e., JJ1886, JJ1887, JJ2547, CU758, CU799, and CD364 (which in Price et al was labeled as CD449). Dates are shown for the 2 households that underwent serial sampling (households 4 and 6). Clustering by household supports within-household transmission (strain sharing); near identify of clinical and fecal isolates within each household supports the fecal reservoir as the source for infection-causing strains; and variation in a given strain within its source household over time (households 4 and 5) suggests microevolution during long-term host colonization. Reprinted from reference 63 , with permission.

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017
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Tables

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Table 1

Virulence-associated traits of extraintestinal pathogenic (ExPEC) by functional category

Citation: Johnson J, Russo T. 2018. Molecular Epidemiology of Extraintestinal Pathogenic , EcoSal Plus 2018; doi:10.1128/ecosalplus.ESP-0004-2017

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