Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns

ABSTRACT The spatiotemporal variation of several carbapenemase-encoding genes (CRGs) was investigated in the influent and effluent of municipal WWTPs, with or without hospital sewage input. Correlations among gene abundances, bacterial community composition, and wastewater quality parameters were te...

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Main Authors: Adela Teban-Man, Edina Szekeres, Peiju Fang, Uli Klümper, Adriana Hegedus, Andreea Baricz, Thomas Ulrich Berendonk, Marcel Pârvu, Cristian Coman
Format: Article
Language:English
Published: American Society for Microbiology 2022-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02711-21
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author Adela Teban-Man
Edina Szekeres
Peiju Fang
Uli Klümper
Adriana Hegedus
Andreea Baricz
Thomas Ulrich Berendonk
Marcel Pârvu
Cristian Coman
author_facet Adela Teban-Man
Edina Szekeres
Peiju Fang
Uli Klümper
Adriana Hegedus
Andreea Baricz
Thomas Ulrich Berendonk
Marcel Pârvu
Cristian Coman
author_sort Adela Teban-Man
collection DOAJ
description ABSTRACT The spatiotemporal variation of several carbapenemase-encoding genes (CRGs) was investigated in the influent and effluent of municipal WWTPs, with or without hospital sewage input. Correlations among gene abundances, bacterial community composition, and wastewater quality parameters were tested to identify possible predictors of CRGs presence. Also, the possible role of wastewaters in mirroring clinical resistance is discussed. The taxonomic groups and gene abundances showed an even distribution among wastewater types, meaning that hospital sewage does not influence the microbial diversity and the CRG pool. The bacterial community was composed mainly of Proteobacteria, Firmicutes, Actinobacteria, Patescibacteria, and Bacteroidetes. Acinetobacter spp. was the most abundant group and had the majority of operational taxonomic units (OTUs) positively correlated with CRGs. This agrees with recent reports on clinical data. The influent samples were dominated by blaKPC, as opposed to effluent, where blaIMP was dominant. Also, blaIMP was the most frequent CRG family observed to correlate with bacterial taxa, especially with the Mycobacterium genus in effluent samples. Bacterial load, blaNDM, blaKPC, and blaOXA-48 abundances were positively correlated with BOD5, TSS, HEM, Cr, Cu, and Fe concentrations in wastewaters. When influent gene abundance values were converted into population equivalent (PE) data, the highest copies/1 PE were identified for blaKPC and blaOXA-48, agreeing with previous studies regarding clinical isolates. Both hospital and non-hospital-type samples followed a similar temporal trend of CRG incidence, but with differences among gene groups. Colder seasons favored the presence of blaNDM, blaKPC and blaOXA-48, whereas warmer temperatures show increased PE values for blaVIM and blaIMP. IMPORTANCE Wastewater-based epidemiology has recently been recognized as a valuable, cost-effective tool for antimicrobial resistance surveillance. It can help gain insights into the characteristics and distribution of antibiotic resistance elements at a local, national, and even global scale. In this study, we investigated the possible use of municipal wastewaters in the surveillance of clinically relevant carbapenemase-encoding genes (CRGs), seen as critical antibiotic resistance determinants. In this matter, our results highlight positive correlations among CRGs, microbial diversity, and wastewater physical and chemical parameters. Identified predictors can provide valuable data regarding the level of raw and treated wastewater contamination with these important antibiotic resistance genes. Also, wastewater-based gene abundances were used for the first time to observe possible spatiotemporal trends of CRGs incidence in the general population. Therefore, possible hot spots of carbapenem resistance could be easily identified at the community level, surpassing the limitations of health care-associated settings.
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spelling doaj.art-0226cf500e6146b9b14d12eb128350342022-12-22T02:09:15ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-04-0110210.1128/spectrum.02711-21Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance PatternsAdela Teban-Man0Edina Szekeres1Peiju Fang2Uli Klümper3Adriana Hegedus4Andreea Baricz5Thomas Ulrich Berendonk6Marcel Pârvu7Cristian Coman8Department of Taxonomy and Ecology, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, RomaniaDepartment of Taxonomy and Ecology, Institute of Biological Research, Branch of NIRDBS, Cluj-Napoca, RomaniaTechnische Universität Dresden, Institute of Hydrobiology, Dresden, GermanyTechnische Universität Dresden, Institute of Hydrobiology, Dresden, GermanyDepartment of Taxonomy and Ecology, Institute of Biological Research, Branch of NIRDBS, Cluj-Napoca, RomaniaDepartment of Taxonomy and Ecology, Institute of Biological Research, Branch of NIRDBS, Cluj-Napoca, RomaniaTechnische Universität Dresden, Institute of Hydrobiology, Dresden, GermanyDepartment of Taxonomy and Ecology, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, RomaniaDepartment of Taxonomy and Ecology, Institute of Biological Research, Branch of NIRDBS, Cluj-Napoca, RomaniaABSTRACT The spatiotemporal variation of several carbapenemase-encoding genes (CRGs) was investigated in the influent and effluent of municipal WWTPs, with or without hospital sewage input. Correlations among gene abundances, bacterial community composition, and wastewater quality parameters were tested to identify possible predictors of CRGs presence. Also, the possible role of wastewaters in mirroring clinical resistance is discussed. The taxonomic groups and gene abundances showed an even distribution among wastewater types, meaning that hospital sewage does not influence the microbial diversity and the CRG pool. The bacterial community was composed mainly of Proteobacteria, Firmicutes, Actinobacteria, Patescibacteria, and Bacteroidetes. Acinetobacter spp. was the most abundant group and had the majority of operational taxonomic units (OTUs) positively correlated with CRGs. This agrees with recent reports on clinical data. The influent samples were dominated by blaKPC, as opposed to effluent, where blaIMP was dominant. Also, blaIMP was the most frequent CRG family observed to correlate with bacterial taxa, especially with the Mycobacterium genus in effluent samples. Bacterial load, blaNDM, blaKPC, and blaOXA-48 abundances were positively correlated with BOD5, TSS, HEM, Cr, Cu, and Fe concentrations in wastewaters. When influent gene abundance values were converted into population equivalent (PE) data, the highest copies/1 PE were identified for blaKPC and blaOXA-48, agreeing with previous studies regarding clinical isolates. Both hospital and non-hospital-type samples followed a similar temporal trend of CRG incidence, but with differences among gene groups. Colder seasons favored the presence of blaNDM, blaKPC and blaOXA-48, whereas warmer temperatures show increased PE values for blaVIM and blaIMP. IMPORTANCE Wastewater-based epidemiology has recently been recognized as a valuable, cost-effective tool for antimicrobial resistance surveillance. It can help gain insights into the characteristics and distribution of antibiotic resistance elements at a local, national, and even global scale. In this study, we investigated the possible use of municipal wastewaters in the surveillance of clinically relevant carbapenemase-encoding genes (CRGs), seen as critical antibiotic resistance determinants. In this matter, our results highlight positive correlations among CRGs, microbial diversity, and wastewater physical and chemical parameters. Identified predictors can provide valuable data regarding the level of raw and treated wastewater contamination with these important antibiotic resistance genes. Also, wastewater-based gene abundances were used for the first time to observe possible spatiotemporal trends of CRGs incidence in the general population. Therefore, possible hot spots of carbapenem resistance could be easily identified at the community level, surpassing the limitations of health care-associated settings.https://journals.asm.org/doi/10.1128/spectrum.02711-21carbapenemaseswastewaterssurveillancewastewater-based epidemiologycarbapenem-resistance genes predictors
spellingShingle Adela Teban-Man
Edina Szekeres
Peiju Fang
Uli Klümper
Adriana Hegedus
Andreea Baricz
Thomas Ulrich Berendonk
Marcel Pârvu
Cristian Coman
Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
Microbiology Spectrum
carbapenemases
wastewaters
surveillance
wastewater-based epidemiology
carbapenem-resistance genes predictors
title Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
title_full Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
title_fullStr Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
title_full_unstemmed Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
title_short Municipal Wastewaters Carry Important Carbapenemase Genes Independent of Hospital Input and Can Mirror Clinical Resistance Patterns
title_sort municipal wastewaters carry important carbapenemase genes independent of hospital input and can mirror clinical resistance patterns
topic carbapenemases
wastewaters
surveillance
wastewater-based epidemiology
carbapenem-resistance genes predictors
url https://journals.asm.org/doi/10.1128/spectrum.02711-21
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