Identification of Diverse Antimicrobial Resistance Determinants Carried on Bacterial, Plasmid, or Viral Metagenomes from an Activated Sludge Microbial Assemblage

Parsley, Larissa C.; Consuegra, Erin J.; Kakirde, Kavita S.; Land, Andrew M.; Harper, Willie F.; Liles, Mark R.

doi:10.1128/aem.03080-09

Cited by 137 publications

(102 citation statements)

References 14 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%

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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

105

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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%

“…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)(8)(9)(10).…”

mentioning

confidence: 99%

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

105

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“…Low-complexity sequence regions (simple sequence repeats) were identified and excluded from consideration during initial pair-wise comparison but were included during final alignment and consensus building. Assembled contigs longer than 10 kb were assigned to their taxonomic affiliations by BLASTN comparisons to the GenBank nonredundant nucleotide (nr/nt) database and selections of the top BLASTN hits for phylogenetic affiliation as described previously (43,44). Clustered regularly interspaced short palindromic repeats (CRISPR) elements were searched from assembled contigs longer than 10 kb by using the Web-based tool CRISPRFinder (18).…”

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confidence: 99%

Metagenomic Analysis of Kimchi, a Traditional Korean Fermented Food

Jung

Lee

Kim

et al. 2011

Appl Environ Microbiol

413

271

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Kimchi, a traditional food in the Korean culture, is made from vegetables by fermentation. In this study, metagenomic approaches were used to monitor changes in bacterial populations, metabolic potential, and overall genetic features of the microbial community during the 29-day fermentation process. Metagenomic DNA was extracted from kimchi samples obtained periodically and was sequenced using a 454 GS FLX Titanium system, which yielded a total of 701,556 reads, with an average read length of 438 bp. Phylogenetic analysis based on 16S rRNA genes from the metagenome indicated that the kimchi microbiome was dominated by members of three genera: Leuconostoc, Lactobacillus, and Weissella. Assignment of metagenomic sequences to SEED categories of the Metagenome Rapid Annotation using Subsystem Technology (MG-RAST) server revealed a genetic profile characteristic of heterotrophic lactic acid fermentation of carbohydrates, which was supported by the detection of mannitol, lactate, acetate, and ethanol as fermentation products. When the metagenomic reads were mapped onto the database of completed genomes, the Leuconostoc mesenteroides subsp. mesenteroides ATCC 8293 and Lactobacillus sakei subsp. sakei 23K genomes were highly represented. These same two genera were confirmed to be important in kimchi fermentation when the majority of kimchi metagenomic sequences showed very high identity to Leuconostoc mesenteroides and Lactobacillus genes. Besides microbial genome sequences, a surprisingly large number of phage DNA sequences were identified from the cellular fractions, possibly indicating that a high proportion of cells were infected by bacteriophages during fermentation. Overall, these results provide insights into the kimchi microbial community and also shed light on fermentation processes carried out broadly by complex microbial communities.

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“…However, CAP is still widely used in low-income countries as it is inexpensive and readily available. Trace levels of CAP (ng to μg level) and novel CAP-resistant bacteria/genes are frequently detected in diverse ecosystems (Leung et al, 2012;Li et al, 2013;Liang et al, 2013;Parsley et al, 2010;Xi et al, 2009;Zhang and Li, 2011;Zhang et al, 2009). Thus, a CAP degradation system with high efficiency is needed to decrease the possibility of evolution of CAP-resistant bacteria/genes in the environment.…”

Section: Introductionmentioning

confidence: 99%

Effect of temperature switchover on the degradation of antibiotic chloramphenicol by biocathode bioelectrochemical system

Kong

Liang

Lee

et al. 2014

Journal of Environmental Sciences

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Identification of Diverse Antimicrobial Resistance Determinants Carried on Bacterial, Plasmid, or Viral Metagenomes from an Activated Sludge Microbial Assemblage

Cited by 137 publications

References 14 publications

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

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

Metagenomic Analysis of Kimchi, a Traditional Korean Fermented Food

Effect of temperature switchover on the degradation of antibiotic chloramphenicol by biocathode bioelectrochemical system

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