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Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

View Article: PubMed Central - PubMed

ABSTRACT

The emergence of resistance to last-resort antibiotics is a public health concern of global scale. Besides direct person-to-person propagation, environmental pathways might contribute to the dissemination of antibiotic-resistant bacteria and antibiotic resistance genes (ARGs). Here, we describe the incidence of blaNDM-1, a gene conferring resistance to carbapenems, in the wastewater of the city of Jeddah, Saudi Arabia, over a 1-year period. blaNDM-1 was detected at concentrations ranging from 104 to 105 copies/m3 of untreated wastewater during the entire monitoring period. These results indicate the ubiquity and high incidence of blaNDM-1 in the local wastewater. To track the bacteria carrying blaNDM-1, we isolated Escherichia coli PI7, a strain of sequence type 101 (ST101), from wastewater around the Hajj event in October 2013. Genome sequencing of this strain revealed an extensive repertoire of ARGs as well as virulence and invasive traits. These traits were further confirmed by antibiotic resistance profiling and in vitro cell internalization in HeLa cell cultures. Given that this strain remains viable even after a certain duration in the sewerage, and that Jeddah lacks a robust sanitary infrastructure to fully capture all generated sewage, the presence of this bacterium in the untreated wastewater represents a potential hazard to the local public health. To the best of our knowledge, this is the first report of a blaNDM-1-positive E. coli strain isolated from a nonnosocomial environment in Saudi Arabia and may set a priority concern for the need to establish improved surveillance for carbapenem-resistant E. coli in the country and nearby regions.

No MeSH data available.


(a) Mapping of genomic islands, pathogenicity factors, and antibiotic resistance loci in the E. coli PI7 genome. Yellow and blue lines represent genomic islands predicted by SIGI-HMM and IslandPath/DIMOB, respectively. Red lines represent the genomic locations of all predicted islands. Asterisks correspond to locations of antibiotic efflux pumps. (b) T3SS gene cluster in E. coli PI7. Green arrows represent structural T3SS genes, pink arrows represent genetic elements associated with gene mobility, and gray arrows represent genes encoding hypothetical proteins (HPs) predicted by Secretome 1.1 for noncanonical secretion signals.
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Figure 3: (a) Mapping of genomic islands, pathogenicity factors, and antibiotic resistance loci in the E. coli PI7 genome. Yellow and blue lines represent genomic islands predicted by SIGI-HMM and IslandPath/DIMOB, respectively. Red lines represent the genomic locations of all predicted islands. Asterisks correspond to locations of antibiotic efflux pumps. (b) T3SS gene cluster in E. coli PI7. Green arrows represent structural T3SS genes, pink arrows represent genetic elements associated with gene mobility, and gray arrows represent genes encoding hypothetical proteins (HPs) predicted by Secretome 1.1 for noncanonical secretion signals.

Mentions: Twenty-four genomic islands (GIs) ranging from 4 to 32 kb were detected in the E. coli PI7 genome. These islands harbor several metabolic and pathogen-associated characteristics, with the most relevant traits depicted in Fig. 3a. The repertoire of pathogenic traits in E. coli PI7 includes the following: (i) the colonization fimbrial antigen I (CFA/I), which has been linked with enterotoxigenic E. coli (ETEC) pathotypes (32); (ii) surface protein OmpA, typically required for cell adhesion and invasion (33); (iii) two intimin-like proteins associated with enterohemorrhagic and enteropathogenic E. coli (EHEC and EPEC, respectively) pathotypes (34); (iv) surface protein IcsA (VirG) required for actin-dependent movement and inter- or intracellular spread in enteroinvasive E. coli (EIEC) and Shigella flexneri (35, 36); (v) an accessory colonization factor (AcfD) previously identified in Vibrio cholerae which facilitates efficient intestinal colonization (37); and (vi) a secondary copy of the type 1 fimbriae located ectopically in a GI and showing >99% amino acid sequence identity with fimbrial clusters of pathogenic E. coli O157:H7 strain EDL933.


Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia
(a) Mapping of genomic islands, pathogenicity factors, and antibiotic resistance loci in the E. coli PI7 genome. Yellow and blue lines represent genomic islands predicted by SIGI-HMM and IslandPath/DIMOB, respectively. Red lines represent the genomic locations of all predicted islands. Asterisks correspond to locations of antibiotic efflux pumps. (b) T3SS gene cluster in E. coli PI7. Green arrows represent structural T3SS genes, pink arrows represent genetic elements associated with gene mobility, and gray arrows represent genes encoding hypothetical proteins (HPs) predicted by Secretome 1.1 for noncanonical secretion signals.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4997845&req=5

Figure 3: (a) Mapping of genomic islands, pathogenicity factors, and antibiotic resistance loci in the E. coli PI7 genome. Yellow and blue lines represent genomic islands predicted by SIGI-HMM and IslandPath/DIMOB, respectively. Red lines represent the genomic locations of all predicted islands. Asterisks correspond to locations of antibiotic efflux pumps. (b) T3SS gene cluster in E. coli PI7. Green arrows represent structural T3SS genes, pink arrows represent genetic elements associated with gene mobility, and gray arrows represent genes encoding hypothetical proteins (HPs) predicted by Secretome 1.1 for noncanonical secretion signals.
Mentions: Twenty-four genomic islands (GIs) ranging from 4 to 32 kb were detected in the E. coli PI7 genome. These islands harbor several metabolic and pathogen-associated characteristics, with the most relevant traits depicted in Fig. 3a. The repertoire of pathogenic traits in E. coli PI7 includes the following: (i) the colonization fimbrial antigen I (CFA/I), which has been linked with enterotoxigenic E. coli (ETEC) pathotypes (32); (ii) surface protein OmpA, typically required for cell adhesion and invasion (33); (iii) two intimin-like proteins associated with enterohemorrhagic and enteropathogenic E. coli (EHEC and EPEC, respectively) pathotypes (34); (iv) surface protein IcsA (VirG) required for actin-dependent movement and inter- or intracellular spread in enteroinvasive E. coli (EIEC) and Shigella flexneri (35, 36); (v) an accessory colonization factor (AcfD) previously identified in Vibrio cholerae which facilitates efficient intestinal colonization (37); and (vi) a secondary copy of the type 1 fimbriae located ectopically in a GI and showing >99% amino acid sequence identity with fimbrial clusters of pathogenic E. coli O157:H7 strain EDL933.

View Article: PubMed Central - PubMed

ABSTRACT

The emergence of resistance to last-resort antibiotics is a public health concern of global scale. Besides direct person-to-person propagation, environmental pathways might contribute to the dissemination of antibiotic-resistant bacteria and antibiotic resistance genes (ARGs). Here, we describe the incidence of blaNDM-1, a gene conferring resistance to carbapenems, in the wastewater of the city of Jeddah, Saudi Arabia, over a 1-year period. blaNDM-1 was detected at concentrations ranging from 104 to 105 copies/m3 of untreated wastewater during the entire monitoring period. These results indicate the ubiquity and high incidence of blaNDM-1 in the local wastewater. To track the bacteria carrying blaNDM-1, we isolated Escherichia coli PI7, a strain of sequence type 101 (ST101), from wastewater around the Hajj event in October 2013. Genome sequencing of this strain revealed an extensive repertoire of ARGs as well as virulence and invasive traits. These traits were further confirmed by antibiotic resistance profiling and in vitro cell internalization in HeLa cell cultures. Given that this strain remains viable even after a certain duration in the sewerage, and that Jeddah lacks a robust sanitary infrastructure to fully capture all generated sewage, the presence of this bacterium in the untreated wastewater represents a potential hazard to the local public health. To the best of our knowledge, this is the first report of a blaNDM-1-positive E. coli strain isolated from a nonnosocomial environment in Saudi Arabia and may set a priority concern for the need to establish improved surveillance for carbapenem-resistant E. coli in the country and nearby regions.

No MeSH data available.