Bacteriophages as a reservoir of extended-spectrum β -lactamase and fluoroquinolone resistance genes in the environment

Marti, Elisabet; Variatza, Eleni; Balcázar, José Luís

doi:10.1111/1469-0691.12446

Cited by 99 publications

(58 citation statements)

References 15 publications

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“…Several studies have detected ARGs in the bacteriophage metagenome (or phageome) of a wide variety of environmental matrices, including activated sludge (9,12), urban sewage and river water (13), and various wastewater effluents from hospitals and wastewater treatment plants (14,26). When specific ARGs are detected by real-time PCR in the bacteriophage populations of the above-described environments, their levels are only about 10-fold lower than those in the corresponding bacterial fractions, on average (reviewed in reference 2).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, bacteriophage from drug-treated mice provided cultured naive microbiota with increased levels of resistance to the corresponding drug. Overall, this work concluded that antibiotic residues potentiate the transduction-mediated dissemination of ARGs.Antibiotic resistance genes have been found in the bacteriophage DNA fraction of various environmental matrices, such as activated sludge (12), urban sewage and river water (13), and wastewater effluents from hospitals and wastewater treatment plants (14). The aforementioned studies indicate that bacteriophage represents a reservoir of ARGs across a broad selection of environments.…”

mentioning

confidence: 99%

“…Antibiotic resistance genes have been found in the bacteriophage DNA fraction of various environmental matrices, such as activated sludge (12), urban sewage and river water (13), and wastewater effluents from hospitals and wastewater treatment plants (14). The aforementioned studies indicate that bacteriophage represents a reservoir of ARGs across a broad selection of environments.…”

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confidence: 99%

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Abundance of Antibiotic Resistance Genes in Bacteriophage following Soil Fertilization with Dairy Manure or Municipal Biosolids, and Evidence for Potential Transduction

Ross

Topp

2015

Appl Environ Microbiol

102

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Animal manures and municipal biosolids recycled onto crop production land carry antibiotic-resistant bacteria that can influence the antibiotic resistome of agricultural soils, but little is known about the contribution of bacteriophage to the dissemination of antibiotic resistance genes (ARGs) in this context. In this work, we quantified a set of ARGs in the bacterial and bacteriophage fractions of agricultural soil by quantitative PCR. All tested ARGs were present in both the bacterial and phage fractions. We demonstrate that fertilization of soil with dairy manure or human biosolids increases ARG abundance in the bacterial fraction but not the bacteriophage fraction and further show that pretreatment of dairy manure can impact ARG abundance in the bacterial fraction. Finally, we show that purified bacteriophage can confer increased antibiotic resistance to soil bacteria when combined with selective pressure. The results indicate that soilborne bacteriophage represents a substantial reservoir of antibiotic resistance and that bacteriophage could play a significant role in the horizontal transfer of resistance genes in the context of an agricultural soil microbiome. Overall, our work reinforces the advisability of composting or digesting fecal material prior to field application and suggests that application of some antibiotics at subclinical concentrations can promote bacteriophage-mediated horizontal transfer of ARGs in agricultural soil microbiomes. Overuse of antibiotics has contributed to the spread of antibiotic resistance due to the release of antibiotics, antibioticresistant bacteria, and antibiotic resistance genes (ARGs) into the environment (1). This phenomenon is mediated by horizontal gene transfer (HGT) of mobile genetic elements-such as plasmids, transposons, and integrons-between bacterial cells through conjugation and viral transduction (2-4).Transduction has been shown to occur in environmental matrices, including freshwater and wastewater; moreover, bacterial 16S ribosomal RNA sequences have been observed in the viral fraction of wastewater, confirming the ability of bacteriophage to carry bacterial genes (5, 6). In fact, while much attention has been paid to conjugation, more recent work has additionally implicated bacteriophage as a major vehicle for horizontal gene transfer and recombination (7-10).Using high-throughput sequencing of murine fecal phage populations, Modi et al. (11) demonstrated that antibiotic treatment leads to the enrichment of genes conferring resistance to the administered drug as well as to unrelated antibiotics in the phage genome. Furthermore, bacteriophage from drug-treated mice provided cultured naive microbiota with increased levels of resistance to the corresponding drug. Overall, this work concluded that antibiotic residues potentiate the transduction-mediated dissemination of ARGs.Antibiotic resistance genes have been found in the bacteriophage DNA fraction of various environmental matrices, such as activated sludge (12), urban sewage and river water (13), an...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Abundance of Antibiotic Resistance Genes in Bacteriophage following Soil Fertilization with Dairy Manure or Municipal Biosolids, and Evidence for Potential Transduction

Ross

Topp

2015

Appl Environ Microbiol

102

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“…In contrast to the previous study, the authors demonstrated that those ARGs ( bla TEM and bla CTX-M ) from phage DNA were transferred to susceptible E. coli strains, which became resistant to ampicillin [9]. Another study of phage DNA from different hospital and urban treated effluents using qPCR assays showed the presence of high levels of genes ( bla TEM , bla CTX-M and bla SHV ) conferring resistance to β-lactam antibiotics, as well as genes ( qnrA , qnrB and qnrS ) conferring reduced susceptibility to fluoroquinolones [10]. Likewise, a recent study demonstrated the presence of the qnrA and qnrS genes in phage DNA from fecally polluted waters and the influence of phage-inducing factors on the abundance of those ARGs.…”

Section: Phages As Vehicles For Antibiotic Resistance Genesmentioning

confidence: 99%

Bacteriophages as Vehicles for Antibiotic Resistance Genes in the Environment

2014

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“…Although transduction is not considered to be the most frequent vehicle for resistance gene transfer, resistance gene sequences have been detected in the viral communities of the human gut, lungs and in the activated sludge of wastewater treatment plants [28,29], all of which are sites of mixing between environmental bacteria and human pathogens. Moreover, antibiotic use can induce phage-mediated transfer [30,31], suggesting that the phage population may emerge as a more frequent vehicle for resistance transfer.…”

Section: Mobile Elements Important For Transfer Between Biomesmentioning

confidence: 99%