Characteristics of Carbapenemase-Producing Enterobacteriaceae in Wastewater Revealed by Genomic Analysis

Gomi, Ryota; Matsuda, Tomonari; Yamamoto, Masaki; Chou, Pei Hsin; Tanaka, Michio; Ichiyama, Satoshi; Yoneda, Minoru; Matsumura, Yasufumi

doi:10.1128/aac.02501-17

Cited by 61 publications

(42 citation statements)

References 63 publications

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“…GES-type beta-lactamases were the second most abundant ESBLs in our study, with several variants capable of low-level hydrolysis of carbapenems [56]. GES-carrying carbapenem-resistant strains have been previously isolated from hospital effluent [57]. GES-type ESBL genes are found globally and exclusively as integron gene cassettes in Gram-negative pathogens, including P. aeruginosa, E. coli, K. pneumoniae, and A. baumannii [58].…”

Section: Discussionmentioning

confidence: 68%

Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

et al. 2019

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Background: Hospital wastewaters contain fecal material from a large number of individuals, of which many are undergoing antibiotic therapy. It is, thus, plausible that hospital wastewaters could provide opportunities to find novel carbapenemases and other resistance genes not yet described in clinical strains. Our aim was therefore to investigate the microbiota and antibiotic resistome of hospital effluent collected from the city of Mumbai, India, with a special focus on identifying novel carbapenemases. Results: Shotgun metagenomics revealed a total of 112 different mobile antibiotic resistance gene types, conferring resistance against almost all classes of antibiotics. Beta-lactamase genes, including encoding clinically important carbapenemases, such as NDM, VIM, IMP, KPC, and OXA-48, were abundant. NDM (0.9% relative abundance to 16S rRNA genes) was the most common carbapenemase gene, followed by OXA-58 (0.84% relative abundance to 16S rRNA genes). Among the investigated mobile genetic elements, class 1 integrons (11% relative abundance to 16S rRNA genes) were the most abundant. The genus Acinetobacter accounted for as many as 30% of the total 16S rRNA reads, with A. baumannii accounting for an estimated 2.5%. High throughput sequencing of amplified integron gene cassettes identified a novel functional variant of an IMP-type (proposed IMP-81) carbapenemase gene (eight aa substitutions) along with recently described novel resistance genes like sul4 and bla RSA1. Using a computational hidden Markov model, we detected 27 unique metallo-beta-lactamase (MBL) genes in the shotgun data, of which nine were novel subclass B1 genes, one novel subclass B2, and 10 novel subclass B3 genes. Six of the seven novel MBL genes were functional when expressed in Escherichia coli. Conclusion: By exploring hospital wastewater from India, our understanding of the diversity of carbapenemases has been extended. The study also demonstrates that the microbiota of hospital wastewater can serve as a reservoir of novel resistance genes, including previously uncharacterized carbapenemases with the potential to spread further.

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Section: Discussionmentioning

confidence: 68%

Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

et al. 2019

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“…Those two patients were individually administered with antibiotics for the infections by other bacteria, and the two strains managed to acquire multidrug resistance through sets of antibiotic treatments. Multidrug resistant bacteria that have been released through facilities such as wastewater handling facilities of hospitals [10], are potentially aerosolized and transported through air or humans that host the strain of non-virulent bacteria as part of their microbiome. Table 1 Genetic distance by MASH and allele and sequence type number by MLST Sequence type of the house-keeping genes were defined through PubMLST.org using database for E. cloacae.…”

Section: Discussionmentioning

confidence: 99%

“…It has been reported that the gut microbiome community of healthy volunteers administered with cefprozil, one of beta-lactam antibiotics, drifts towards a higher abundance of antibiotic resistant bacteria including ECC [8]. The affected gut microbiota can end up in the sewage of hospitals, and turn the wastewater facilities into a reservoir for antibiotic resistant bacteria [9,10]. As such, there is an increasing risk of spreading multidrug resistant strains and associated genes by releasing them into the environment through wastewater and other means [10].…”

Section: Gut Pathogensmentioning

confidence: 99%

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Complete genome of Enterobacter sichuanensis strain SGAir0282 isolated from air in Singapore

et al. 2020

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Background: Enterobacter cloacae complex (ECC) bacteria, such as E. cloacae, E. sichuanensis, E. kobei, and E. roggenkampii, have been emerging as nosocomial pathogens. Many strains isolated from medical clinics were found to be resistant to antibiotics, and in the worst cases, acquired multidrug resistance. We present the whole genome sequence of SGAir0282, isolated from the outdoor air in Singapore, and its relevance to other ECC bacteria by in silico genomic analysis. Results: Complete genome assembly of E. sichuanensis strain SGAir0282 was generated using PacBio RSII and Illumina MiSeq platforms, and the datasets were used for de novo assembly using Hierarchical Genome Assembly Process (HGAP) and error corrected with Pilon. The genome assembly consisted of a single contig of 4.71 Mb and with a G+C content of 55.5%. No plasmid was detected in the assembly. The genome contained 4371 coding genes, 83 tRNA and 25 rRNA genes, as predicted by NCBI's Prokaryotic Genome Annotation Pipeline (PGAP). Among the genes, the antibiotic resistance related genes were included: Streptothricin acetdyltransferase (SatA), fosfomycin resistance protein (FosA) and metal-dependent hydrolases of the beta-lactamase superfamily I (BLI). Conclusion: Based on whole genome alignment and phylogenetic analysis, the strain SGAir0282 was identified to be Enterobacter sichuanensis. The strain possesses gene clusters for virulence, disease and defence, that can also be found in other multidrug resistant ECC type strains.

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“…As seen here, it is not readily distinguished from K. pneumoniae with current clinical microbiology techniques and thus the true prevalence is unknown(2, 22). On the evolutionary time scale, modern medicine has provided a novel ecology with immunocompromised patients, widespread antimicrobial use, newly circulating antimicrobial resistance genes and the design of the modern hospital providing new microbiologic niche for organisms to emerge(7, 23). As seen here we provide evidence for K. quasipneumoniae to be sustained in both a human host and the environment encountering several different species which may be relatively new in the evolutionary tree of Klebsiella sp.…”

Section: Discussionmentioning

confidence: 99%

Klebsiella quasipneumonaiae provides a window into carbapenemase gene transfer, plasmid rearrangements and nosocomial acquisition from the hospital environment

Mathers

Crook

Vaughan

et al. 2018

Preprint

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22Several emerging pathogens have arisen as a result of selection pressures exerted by modern healthcare. 23Klebsiella quasipneumoniae was recently defined as a new species, yet its prevalence, niche, and propensity to 24 acquire antimicrobial resistance genes are not fully described. We have been tracking inter-and intra-species 25 transmission of the Klebsiella pneumoniae carbapenemase (KPC) gene, bla KPC , between bacteria isolated from a 26 single institution. We applied a combination of Illumina and PacBio whole-genome sequencing to identify and 27 compare K. quasipneumoniae from patients and the hospital environment over 10 and five-year periods 28respectively. There were 32 bla KPC -positive K. quasipneumoniae isolates, all of which were identified as K. 29 pneumoniae in the clinical microbiology laboratory, from eight patients and 11 sink drains, with evidence for 30 seven separate bla KPC plasmid acquisitions. Analysis of a single subclade of K. quasipneumoniae subspecies 31 quasipneumoniae (n=23 isolates) from three patients and six rooms demonstrated seeding of a sink by a patient, 32 subsequent persistence of the strain in the hospital environment, and then probable transmission to another 33 patient. Longitudinal analysis of this strain demonstrated the acquisition of two unique bla KPC plasmids and then 34 subsequent within-strain genetic rearrangement through transposition and homologous recombination. Our 35 analysis highlights the apparent molecular propensity of K. quasipneumoniae to persist in the environment as well 36as acquire carbapenemase plasmids from other species and enabled an assessment of the genetic rearrangements 37

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Characteristics of Carbapenemase-Producing Enterobacteriaceae in Wastewater Revealed by Genomic Analysis

Cited by 61 publications

References 63 publications

Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

Complete genome of Enterobacter sichuanensis strain SGAir0282 isolated from air in Singapore

Klebsiella quasipneumonaiae provides a window into carbapenemase gene transfer, plasmid rearrangements and nosocomial acquisition from the hospital environment

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