A population genomics approach to exploiting the accessory 'resistome' of Escherichia coli

Goldstone, Robert; Smith, David George Emslie

doi:10.1099/mgen.0.000108

Cited by 19 publications

(19 citation statements)

References 87 publications

(50 reference statements)

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“…This revealed an exceptionally high prevalence of accessory antibiotic resistances among O89m strains which was supplemented through substitutions in GyrA, GyrB, ParE, and ParC consistent with quinolone resistance. Greater than 95% of O89m strains showed carriage of one or more accessory resistance determinant compared to approximately 50% of E. coli as an entire population ( Goldstone and Smith, 2017 ). Resistances for aminoglycosides, sulphonamides, tetracycline, or β-lactams/cephalosporins were most common, each being detected in >80% of O89m strains.…”

Section: Resultsmentioning

confidence: 99%

“…Most (90%) O89m strains can be classified as MDR (three or more resistances) and the mean, median and modal values for resistance classes were 6, 7, and 8, respectively. In contrast, O89 strains showed mean, median and modal values of 1, 1, and 0, respectively, and for E. coli as an entire population these values were 1.6, 0, and 0, respectively ( Goldstone and Smith, 2017 ). Among O89m isolates, 118 (58%) carried either extended-spectrum β-lactamases (ESBLs) or carbapenemases of CTX-M, CMY, SHV, NDM, KPC or OXA-48 classes.…”

Section: Resultsmentioning

confidence: 99%

“…Specifically, the O89 strains typically carried zero or one resistance (although two O89 strains can be categorized as multidrug resistant) whilst 89% of the O89m strains can be categorized as MDR with these strains carrying resistance to an average of six antibiotic classes. Carriage of this magnitude of resistances resembles the accumulation of resistances in ST131 strains ( Pitout and DeVinney, 2017 ) although it is unusual among the entirety of E. coli ( Goldstone and Smith, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

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Variant O89 O-Antigen of E. coli Is Associated With Group 1 Capsule Loci and Multidrug Resistance

et al. 2018

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Bacterial surface polysaccharides play significant roles in fitness and virulence. In Gram-negative bacteria such as Escherichia coli, major surface polysaccharides are lipopolysaccharide (LPS) and capsule, representing O- and K-antigens, respectively. There are multiple combinations of O:K types, many of which are well-characterized and can be related to ecotype or pathotype. In this investigation, we have identified a novel O:K permutation resulting through a process of major genome reorganization in a clade of E. coli. A multidrug-resistant, extended-spectrum β-lactamase (ESBL)-producing strain – E. coli 26561 – represented a prototype of strains combining a locus variant of O89 and group 1 capsular polysaccharide. Specifically, the variant O89 locus in this strain was truncated at gnd, flanked by insertion sequences and located between nfsB and ybdK and we apply the term O89m for this variant. The prototype lacked colanic acid and O-antigen loci between yegH and hisI with this tandem polysaccharide locus being replaced with a group 1 capsule (G1C) which, rather than being a recognized E. coli capsule type, this locus matched to Klebsiella K10 capsule type. A genomic survey identified more than 200 E. coli strains which possessed the O89m locus variant with one of a variety of G1C types. Isolates from our collection with the combination of O89m and G1C all displayed a mucoid phenotype and E. coli 26561 was unusual in exhibiting a mucoviscous phenotype more recognized as a characteristic among Klebsiella strains. Despite the locus truncation and novel location, all O89m:G1C strains examined showed a ladder pattern typifying smooth LPS and also showed high molecular weight, alcian blue-staining polysaccharide in cellular and/or extra-cellular fractions. Expression of both O-antigen and capsule biosynthesis loci were confirmed in prototype strain 26561 through quantitative proteome analysis. Further in silico exploration of more than 200 E. coli strains possessing the O89m:G1C combination identified a very high prevalence of multidrug resistance (MDR) – 85% possessed resistance to three or more antibiotic classes and a high proportion (58%) of these carried ESBL and/or carbapenemase. The increasing isolation of O89m:G1C isolates from extra-intestinal infection sites suggests that these represents an emergent clade of invasive, MDR E. coli.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Variant O89 O-Antigen of E. coli Is Associated With Group 1 Capsule Loci and Multidrug Resistance

et al. 2018

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“…Hence, most of the evolution of the species takes place in biotic contexts not associated with pathogenesis. Furthermore, while a lot of attention has been placed on the rates of homologous recombination in the chromosome of the species, it is now clear that HGT drives the evolution of virulence 12, 42, 68, 69 and antibiotic resistance 70–72 in pathogenic strains as well as that of many other traits in commensal strains 12 . For example, MGEs were recently shown to be more important than point mutations for the colonization of the mouse gut by E. coli commensals 73 .…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic background and habitat drive the genetic diversification ofEscherichia coli

Touchon

Amandine

Sousa

et al. 2020

Preprint

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23Escherichia coli is a commensal of birds and mammals, including humans. It can act as an 24 opportunistic pathogen and is also found in water and sediments. Since most population 25 studies have focused on clinical isolates, we studied the phylogeny, genetic diversification, 26 and habitat-association of 1,294 isolates representative of the phylogenetic diversity of more 27 than 5,000, mostly non-clinical, isolates originating from humans, poultry, wild animals and 28 water sampled from the Australian continent. These strains represent the species diversity 29 and show large variations in gene repertoires within sequence types. Recent gene transfer is 30 driven by mobile elements and determined by habitat sharing and by phylogroup 31 membership, suggesting that gene flow reinforces the association of certain genetic 32 backgrounds with specific habitats. The phylogroups with smallest genomes had the highest 33 rates of gene repertoire diversification and fewer but more diverse mobile genetic elements, 34 suggesting that smaller genomes are associated with higher, not lower, turnover of genetic 35 information. Many of these small genomes were in freshwater isolates suggesting that some 36 lineages are specifically adapted to this environment. Altogether, these data contribute to 37 explain why epidemiological clones tend to emerge from specific phylogenetic groups in the 38 presence of pervasive horizontal gene transfer across the species. 39 40 circulation of strains and the high plasticity of their genomes have not erased the 68 associations of certain clades with certain isolation sources. In consequence, such 69 associations might reflect local adaptation 16,45 , which would suggest frequent genetic 70 interactions between the novel adaptive changes and the strains' genomic background. 71Understanding how the evolution of gene repertoires is shaped by population structure and 72 habitats requires large-scale comparative genomics of samples with diverse sources of 73 isolation representative of natural populations of E. coli. Most of the efforts of genome 74 sequencing have been devoted to study pathogenic lineages and very few genomic data are 75 available for commensal strains, especially in wild animals, and environmental strains. Here, 76we analysed the genomes of a large collection of E. coli strains collected across many 77 human, domestic and wild animal and environmental sources in different geographic 78 locations from the Australian continent. This collection is dominated by non-clinical isolates, 79 corresponding to the main habitats of the species. We sought to understand the dynamics of 80 the evolution of gene repertoires and how it was driven by mobile genetic elements. The 81 analysis of the isolation sources in the light of phylogenetic structure and genome variation 82 suggests that adaptation varies with the habitat and the phylogenomic background. This 83 contributes to explain why known epidemiological clones of the species emerge from specific 84 phylogenetic groups, even though virulen...

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“…The ST131 resistome (the set of AMR genes) includes ESBL genes [33][34] allowing third-generation cephalosporin-resistance [35] and are associated with three main cefotaximase (CTX-M) resistance alleles: blaCTX-M-14/15/27 [36]. Like most AMR genes, these are sandwiched by mobile genetic elements (MGEs) on plasmids and thus can be gained by horizontal gene transfer (HGT) [37][38][39] or lost if not beneficial [40][41]. Of nine common bacterial pathogens, E. coli has the most MGEs, including phageassociated ones and transpose (tnpA) genes [42].…”

Section: Introductionmentioning

confidence: 99%

Plasmids shape the diverse accessory resistomes ofEscherichia coliST131

Decano

Tran

Al-Foori

et al. 2020

Preprint

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19The human gut microbiome includes beneficial, commensal and pathogenic bacteria that possess 20 antimicrobial resistance (AMR) genes and exchange these predominantly through conjugative 21 plasmids. Escherichia coli is a significant component of the gastrointestinal microbiome and is 22typically non-pathogenic in this niche. In contrast, extra-intestinal pathogenic E. coli (ExPEC) 23including ST131 may occupy other environments like the urinary tract or bloodstream where they 24 express genes enabling AMR and host adhesion like type 1 fimbriae. The extent to which non-25pathogenic gut E. coli and infectious ST131 share AMR genes and key associated plasmids remains 26understudied at a genomic level. Here, we examined AMR gene sharing between gut E. coli and 27 ST131 to discover an extensive shared preterm infant resistome. In addition, individual ST131 show 28 extensive AMR gene diversity highlighting that analyses restricted to the core genome may be limiting 29and could miss AMR gene transfer patterns. We show that pEK499-like segments are ancestral to most 30 ST131 Clade C isolates, contrasting with a minority with substantial pEK204-like regions encoding a 31type IV fimbriae operon. Moreover, ST131 possess extensive diversity at genes encoding type 1, type 32 IV, P and F17-like fimbriae, particular within subclade C2. The type, structure and composition of 33 AMR genes, plasmids and fimbriae varies widely in ST131 and this may mediate pathogenicity and 34 infection outcomes. 35 36

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A population genomics approach to exploiting the accessory 'resistome' of Escherichia coli

Cited by 19 publications

References 87 publications

Variant O89 O-Antigen of E. coli Is Associated With Group 1 Capsule Loci and Multidrug Resistance

Variant O89 O-Antigen of E. coli Is Associated With Group 1 Capsule Loci and Multidrug Resistance

Phylogenetic background and habitat drive the genetic diversification ofEscherichia coli

Plasmids shape the diverse accessory resistomes ofEscherichia coliST131

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