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Population Phylogenomics of Extraintestinal Pathogenic

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  • Authors: Jérôme Tourret1, Erick Denamur3
  • Editors: Matthew A. Mulvey4, Ann E. Stapleton5, David J. Klumpp6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Département d’Urologie, Néphrologie et Transplantation Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, Université Pierre et Marie Curie; 2: UMR 1137 INSERM and Université Paris Diderot, IAME, Sorbonne Paris Cité, 75018 Paris, France; 3: UMR 1137 INSERM and Université Paris Diderot, IAME, Sorbonne Paris Cité, 75018 Paris, France; 4: University of Utah, Salt Lake City, UT; 5: University of Washington, Seattle, WA; 6: Northwestern University, Chicago, IL
  • Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
  • Received 09 August 2012 Accepted 23 July 2015 Published 07 January 2016
  • Erick Denamur, erick.denamur@inserm.fr
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  • Abstract:

    The emergence of genomics over the last 10 years has provided new insights into the evolution and virulence of extraintestinal . By combining population genetics and phylogenetic approaches to analyze whole-genome sequences, it became possible to link genomic features to specific phenotypes, such as the ability to cause urinary tract infections. An chromosome can vary extensively in length, ranging from 4.3 to 6.2 Mb, encoding 4,084 to 6,453 proteins. This huge diversity is structured as a set of less than 2,000 genes (core genome) that are conserved between all the strains and a set of variable genes. Based on the core genome, the history of the species can be reliably reconstructed, revealing the recent emergence of phylogenetic groups A and B1 and the more ancient groups B2, F, and D. Urovirulence is most often observed in B2/F/D group strains and is a multigenic process involving numerous combinations of genes and specific alleles with epistatic interactions, all leading down multiple evolutionary paths. The genes involved mainly code for adhesins, toxins, iron capture systems, and protectins, as well as metabolic pathways and mutation-rate-control systems. However, the barrier between commensal and uropathogenic strains is difficult to draw as the factors that are responsible for virulence have probably also been selected to allow survival of as a commensal in the intestinal tract. Genomic studies have also demonstrated that infections are not the result of a unique and stable isolate, but rather often involve several isolates with variable levels of diversity that dynamically changes over time.

  • Citation: Tourret J, Denamur E. 2016. Population Phylogenomics of Extraintestinal Pathogenic . Microbiol Spectrum 4(1):UTI-0010-2012. doi:10.1128/microbiolspec.UTI-0010-2012.

Key Concept Ranking

Type 1 Fimbriae
0.45172527
Hemolytic Uremic Syndrome
0.43888032
Urinary Tract Infections
0.43563992
Pulsed-Field Gel Electrophoresis
0.42978436
0.45172527

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/content/journal/microbiolspec/10.1128/microbiolspec.UTI-0010-2012
2016-01-07
2017-09-25

Abstract:

The emergence of genomics over the last 10 years has provided new insights into the evolution and virulence of extraintestinal . By combining population genetics and phylogenetic approaches to analyze whole-genome sequences, it became possible to link genomic features to specific phenotypes, such as the ability to cause urinary tract infections. An chromosome can vary extensively in length, ranging from 4.3 to 6.2 Mb, encoding 4,084 to 6,453 proteins. This huge diversity is structured as a set of less than 2,000 genes (core genome) that are conserved between all the strains and a set of variable genes. Based on the core genome, the history of the species can be reliably reconstructed, revealing the recent emergence of phylogenetic groups A and B1 and the more ancient groups B2, F, and D. Urovirulence is most often observed in B2/F/D group strains and is a multigenic process involving numerous combinations of genes and specific alleles with epistatic interactions, all leading down multiple evolutionary paths. The genes involved mainly code for adhesins, toxins, iron capture systems, and protectins, as well as metabolic pathways and mutation-rate-control systems. However, the barrier between commensal and uropathogenic strains is difficult to draw as the factors that are responsible for virulence have probably also been selected to allow survival of as a commensal in the intestinal tract. Genomic studies have also demonstrated that infections are not the result of a unique and stable isolate, but rather often involve several isolates with variable levels of diversity that dynamically changes over time.

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Image of FIGURE 1
FIGURE 1

Phylogenetic history, reconstructed from 8 concatenated partial-gene sequences using the Pasteur Institut MLST schema ( 67 ), of 128 strains rooted on . The strains have been chosen to be representative of the species’ genetic diversity and life-styles. They originate from the ECOR collection ( 170 ), our laboratory collection ( 77 ), and from complete genomes available in GenBank. No clade strain is represented, see ( 21 ) for their phylogeny. The strains with a black dot correspond to the strains discussed in the text for which a complete-genome sequence is available. The phylogenetic groups and subgroups (ST complexes) are indicated [see the main text for the correspondence with the ST complexes of ( 19 )]. The EPEC strain E2348/69 belongs to the EPEC-1 group. The arrows indicate 3 famous archetypal strains: the O157:H7 EHEC strain, the laboratory-derived K-12 strain, and the O104:H4 Shiga toxin-producing strain from the 2011 German outbreak, belonging to the E, A, and B1 phylogenetic groups, respectively. This phylogeny is similar to the one obtained from core genomes (data not shown).

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
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Image of FIGURE 2
FIGURE 2

Analysis of the presence of genes in 20 genomes of ( 16 ). The number of genes present in 1 to 20 (all) genomes is presented. The genes that are present in the 20 genomes represent the core genome (11% of the pan-genome), whereas the genes present in only one strain are strain-specific (51% of the pan-genome). It can be seen that very few genes are between these two extremes. When the genes are categorized according to their origin and functions, it appears that strain-specific genes are mostly from mobile elements and of unknown functions, whereas the core-genome genes are almost exclusively composed of non-mobile genes of known functions. Although some of the strain-specific genes confer adaptive functions as discussed in the text, most of these genes are non-adaptive and thus purged over time ( 16 ).

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
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Image of FIGURE 3
FIGURE 3

Schematic representation of two distinct evolutionary scenarios leading to association of a character with virulence. P is for pathogenic (black circle) whereas C stands for commensal (white circle). The character can be the presence of a gene or an allele within a gene. In A, the character has been acquired by chance once in the ancestor of the black strains (red arrow) and is a phylogenetic marker. In B, several independent acquisitions of the character are observed (red arrows), representing a convergence and indicating that this character has been selected and is involved in virulence. The same reasoning can be applied for the loss of a character; in this case the ancestral status is the presence of the character.

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
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FIGURE 4

Schematic representation of interactions between bacterial-associated genotypic factors, host-related conditions, and the resulting clinical syndrome. Highly virulent phylogroup B2 strains can be responsible for severe clinical syndromes in patients with no medical conditions, such as pyelonephritis, urosepsis, or prostatitis. They are highly lethal to mice. NB: These strains can also be found as fecal commensals, a situation that can be explained by the “virulence by-product of commensalism” hypothesis. A/B1 phylogenetic-group strains can be responsible for a severe clinical syndrome in debilitated patients. However, they show little lethality in a mouse model measuring intrinsic virulence. In patients with no medical condition, phylogroup A/B1 strains with little virulence potential are usually found in less-severe conditions such as cystitis, asymptomatic bacteriuria, or even in non-pathogenic fecal samples. They do not show any virulence in a mouse model measuring intrinsic virulence. NB: Some B2 strains with reductive evolution inactivating numerous virulence determinants can also cause ABU. These strains are not lethal in the mouse model of septicemia (E. Denamur, personal data). Depending on the virulence-factors/host-condition combination, highly virulent B2 phylogroup strains can also be responsible for a non-severe clinical syndrome, such as cystitis. Such strains show high intrinsic virulence in a mouse model of septicemia. VFs: virulence factors. ABU: asymptomatic bacteriuria. A, B1, B2, D: phylogenetic groups.

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
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