High Diversity of CTX-M Extended-Spectrum β-Lactamases in Municipal Wastewater and Urban Wetlands

Borgogna, Timothy R.; Borgogna, Joanna-Lynn; Mielke, Jenna A.; Brown, Celeste J.; Top, Eva M.; Botts, Ryan T.; Cummings, David E.

doi:10.1089/mdr.2015.0197

Cited by 11 publications

(13 citation statements)

References 65 publications

(72 reference statements)

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“…Isolation of bla CTX-M containing strains from samples taken in November 2014, December 2014 and January 2015 together with amplification in standard PCR demonstrated that microbes harboring this gene were present at Awba at several time points. The absolute and relative abundances of bla CTX-M-1 measured at the site were similar to that reported for the sediment of Lake Brêt, Switzerland [81], an urban river in Kinshasa, Democratic Republic of Congo [82], and in waste water treatments plants and urban wetlands in the United States [83], but slightly lower than that measured in a river receiving hospital effluents in Tamil Nadu, India [84]. In all of those studies primers targeting Group 1 bla CTX-M were used.…”

Section: Abundances Of Marker Genes In the Wetlandssupporting

confidence: 77%

A survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in urban wetlands in southwestern Nigeria as a step towards generating prevalence maps of antimicrobial resistance

et al. 2020

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In many countries, emission of insufficiently treated wastewater into water bodies appears to be an important factor in spreading clinically relevant antimicrobial resistant bacteria. In this study, we looked for the presence of Enterobacteriaceae strains with resistance to 3 rd generation cephalosporin antibiotics in four urban wetlands in southwestern Nigeria by isolation, whole genome sequencing and qPCR enumeration of marker genes. Genome analysis of multi-drug resistant and potentially pathogenic Escherichia coli isolates (members of the widely distributed ST10 complex) revealed the presence of the extended spectrum beta-lactamase gene bla CTX-M-15 on self-transmissible IncF plasmids. The gene was also present together with a bla TEM-1B gene on self-transmissible IncH plasmids in multi-drug resistant Enterobacter cloacae isolates. A Citrobacter freundii isolate carried bla TEM-1B on an IncRtype plasmid without discernable conjugation apparatus. All strains were isolated from a wetland for which previous qPCR enumeration of marker genes, in particular the ratio of intI1 to 16S rRNA gene copy numbers, had indicated a strong anthropogenic impact. Consistent with the isolation origin, qPCR analysis in this study showed that the bla CTX-M gene was present at an abundance of 1x10 -4 relative to bacterial 16S rRNA gene copy numbers.The results indicate that contamination of these urban aquatic ecosystems with clinically relevant antibiotic resistant bacteria is substantial in some areas. Measures should therefore be put in place to mitigate the propagation of clinically relevant antimicrobial resistance within the Nigerian aquatic ecosystems. PLOS ONEPLOS ONE | https://doi.org/10.

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Section: Abundances Of Marker Genes In the Wetlandssupporting

confidence: 77%

A survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in urban wetlands in southwestern Nigeria as a step towards generating prevalence maps of antimicrobial resistance

et al. 2020

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“…Metagenomic studies suggest that waste water carries a tremendous diversity of novel plasmids that have the potential to recombine with one another, creating raw material upon which natural selection may act ( Sentchilo et al, 2013 ). Release of these genes into the natural environment via sewage has been reported by our lab ( Cummings et al, 2011 ; Borgogna et al, 2016 ) and others ( Novais et al, 2005 ; Zhang et al, 2009 ).…”

Section: Introductionsupporting

confidence: 67%

“…This renders the cephalosporins useless ( Pitout and Laupland, 2008 ; Sheng et al, 2013 ) and forces clinicians to use less desirable alternatives such as carbapenems or polymyxins ( Papp-Wallace et al, 2011 ). In an earlier study, we discovered bla CTX-M genes from phylogenetic groups 1 and 2 in local WWTPs, and group 1 bla CTX-M genes in the TRE sediments during the rainy season ( Borgogna et al, 2016 ). Although their peak abundance (4.39 × 10 -5 copies per 16S rRNA gene) was lower than that seen for qnrA (2.10 × 10 -2 copies per 16S rRNA gene), their diversity was tremendous.…”

Section: Discussionmentioning

confidence: 98%

Characterization of Four Multidrug Resistance Plasmids Captured from the Sediments of an Urban Coastal Wetland

et al. 2017

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Self-transmissible and mobilizable plasmids contribute to the emergence and spread of multidrug-resistant bacteria by enabling the horizontal transfer of acquired antibiotic resistance. The objective of this study was to capture and characterize self-transmissible and mobilizable resistance plasmids from a coastal wetland impacted by urban stormwater runoff and human wastewater during the rainy season. Four plasmids were captured, two self-transmissible and two mobilizable, using both mating and enrichment approaches. Plasmid genomes, sequenced with either Illumina or PacBio platforms, revealed representatives of incompatibility groups IncP-6, IncR, IncN3, and IncF. The plasmids ranged in size from 36 to 144 kb and encoded known resistance genes for most of the major classes of antibiotics used to treat Gram-negative infections (tetracyclines, sulfonamides, β-lactams, fluoroquinolones, aminoglycosides, and amphenicols). The mobilizable IncP-6 plasmid pLNU-11 was discovered in a strain of Citrobacter freundii enriched from the wetland sediments with tetracycline and nalidixic acid, and encodes a novel AmpC-like β-lactamase (blaWDC-1), which shares less than 62% amino acid sequence identity with the PDC class of β-lactamases found in Pseudomonas aeruginosa. Although the IncR plasmid pTRE-1611 was captured by mating wetland bacteria with P. putida KT2440 as recipient, it was found to be mobilizable rather than self-transmissible. Two self-transmissible multidrug-resistance plasmids were also captured: the small (48 kb) IncN3 plasmid pTRE-131 was captured by mating wetland bacteria with Escherichia coli HY842 where it is seemed to be maintained at nearly 240 copies per cell, while the large (144 kb) IncF plasmid pTRE-2011, which was isolated from a cefotaxime-resistant environmental strain of E. coli ST744, exists at just a single copy per cell. Furthermore, pTRE-2011 bears the globally epidemic blaCTX-M-55 extended-spectrum β-lactamase downstream of ISEcp1. Our results indicate that urban coastal wetlands are reservoirs of diverse self-transmissible and mobilizable plasmids of relevance to human health.

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“…Interestingly, for the CTX-M Group 1 ESBLs detected in our study, variants found in the first processing scenario included bla CTX−M−1 and bla CTX−M−15 from E. coli, K. pneumoniae, and S. fonticola isolated from river, irrigation pivot point water, harvested-and retailed spinach samples, whilst in the second processing scenario, CTX-M Group 1 variants included bla CTX−M−3 , bla CTX−M−206 , and bla CTX−M−12 from S. fonticola and E. asburiae isolated from spinach samples during processing and at retail. Previous studies have reported bla CTX−M−14 and bla CTX−M−15 as the most broadly dispersed in clinical isolates, whilst in environmental isolates, CTX-M Group 1 variants (bla CTX−M−1 and bla CTX−M−3 among other), have been reported (Cantón et al, 2012;Borgogna et al, 2016). Additionally, CTX-M Group 1 variants (bla CTX−M−15 , bla CTX−M−3 , and bla CTX−M−12 ) found in the different Enterobacteriaceae isolates from vegetables corresponded to other studies (Ye et al, 2017;Richter et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Occurrence, Phenotypic and Molecular Characterization of Extended-Spectrum- and AmpC- β-Lactamase Producing Enterobacteriaceae Isolated From Selected Commercial Spinach Supply Chains in South Africa

et al. 2020

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The increasing occurrence of multidrug-resistant (MDR) extended-spectrum β-lactamase-(ESBL) and/or AmpC β-lactamase-producing Enterobacteriaceae in health care systems, the environment and fresh produce is a serious concern globally. Production practices, processing and subsequent consumption of contaminated raw fruit and vegetables represent a possible human transmission route. The purpose of this study was to determine the presence of ESBL/AmpC-producing Enterobacteriaceae in complete spinach supply chains and to characterize the isolated strains phenotypically (antimicrobial resistance profiles) and genotypically (ESBL/AmpC genetic determinants, detection of class 1, 2, and 3 integrons). Water, soil, fresh produce, and contact surface samples (n = 288) from two commercial spinach production systems were screened for ESBL/AmpC-producing Enterobacteriaceae. In total, 14.58% (42/288) of the samples were found to be contaminated after selective enrichment, plating onto chromogenic media and matrix-assisted laser desorption ionization time-of-flight mass spectrometry identity confirmation of presumptive ESBL/AmpC isolates. This included 15.28% (11/72) water and 12.12% (16/132) harvested-and processed spinach, while 25% (15/60) retail spinach samples were found to be contaminated with an increase in isolate abundance and diversity in both scenarios. Dominant species identified included Serratia fonticola (45.86%), Escherichia coli (20.83%), and Klebsiella pneumoniae (18.75%). In total, 48 (81.36%) isolates were phenotypically confirmed as ESBL/AmpC-producing Enterobacteriaceae of which 98% showed a MDR phenotype. Genotypic characterization (PCR of ESBL/AmpC resistance genes and integrons) further revealed the domination of the CTX-M Group 1 ESBL type, followed by TEM and SHV; whilst the CIT-type was the only plasmid-mediated AmpC genetic determinant detected. Integrons were detected in 79.17% (n = 38) of the confirmed

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High Diversity of CTX-M Extended-Spectrum β-Lactamases in Municipal Wastewater and Urban Wetlands

Cited by 11 publications

References 65 publications

A survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in urban wetlands in southwestern Nigeria as a step towards generating prevalence maps of antimicrobial resistance

A survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in urban wetlands in southwestern Nigeria as a step towards generating prevalence maps of antimicrobial resistance

Characterization of Four Multidrug Resistance Plasmids Captured from the Sediments of an Urban Coastal Wetland

Occurrence, Phenotypic and Molecular Characterization of Extended-Spectrum- and AmpC- β-Lactamase Producing Enterobacteriaceae Isolated From Selected Commercial Spinach Supply Chains in South Africa

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