Dataset Information

A simple model of tetracycline antibiotic resistance in the aquatic environment (with application to the Poudre River).

ABSTRACT: Antibiotic resistance is a major concern, yet it is unclear what causes the relatively high densities of resistant bacteria in the anthropogenically impacted environment. There are various possible scenarios (hypotheses): (A) Input of resistant bacteria from wastewater and agricultural sources is significant, but they do not grow in the environment; (B) Input of resistant bacteria is negligible, but the resistant bacteria (exogenous or endogenous) grow due to the selection pressure of the antibiotic; (C) Exogenous bacteria transfer the resistance to the endogenous bacteria and those grow. This paper presents a simple mechanistic model of tetracycline resistance in the aquatic environment. It includes state variables for tetracyclines, susceptible and resistant bacteria, and particulate and dissolved organic matter in the water column and sediment bed. The antibiotic partitions between freely dissolved, dissolved organic matter (DOM)-bound and solids-bound phases, and decays. Bacteria growth is limited by DOM, inhibited by the antibiotic (susceptible bacteria only) and lower due to the metabolic cost of carrying the resistance (resistant bacteria only). Resistant bacteria can transfer resistance to the susceptible bacteria (conjugation) and lose the resistance (segregation). The model is applied to the Poudre River and can reproduce the major observed (literature data) patterns of antibiotic concentration and resistance. The model suggests observed densities of resistant bacteria in the sediment bed cannot be explained by input (scenario A), but require growth (scenarios B or C).

SUBMITTER: Hellweger FL

PROVIDER: S-EPMC3084473 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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A simple model of tetracycline antibiotic resistance in the aquatic environment (with application to the Poudre River).

Hellweger Ferdi L FL Ruan Xiaodan X Sanchez Sarah S

International journal of environmental research and public health 20110215 2

Antibiotic resistance is a major concern, yet it is unclear what causes the relatively high densities of resistant bacteria in the anthropogenically impacted environment. There are various possible scenarios (hypotheses): (A) Input of resistant bacteria from wastewater and agricultural sources is significant, but they do not grow in the environment; (B) Input of resistant bacteria is negligible, but the resistant bacteria (exogenous or endogenous) grow due to the selection pressure of the antibi ...[more]

PMID: 21556198

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Project description:The entry of antibiotic resistance genes (ARGs) into aquatic systems has been documented for large municipal wastewater treatment plants (WWTPs), but there is less study of the impact of smaller plants that are situated on small rural rivers. We sampled water metagenomes for ARGs and taxa composition from the Kokosing River, a small rural river in Knox County, Ohio, which has been designated an Ohio State Scenic River for retention of natural character. Samples were obtained 1.0 km upstream, 120 m downstream, and 6.4 km downstream from the effluent release of the Mount Vernon WWTP. ARGs were identified in metagenomes using ShortBRED markers from the comprehensive antibiotic resistance database (CARD) screened against UniPROT. Through all seasons, the metagenome just downstream of the WWTP effluent showed a substantial elevation of at least 15 different ARGs, including 6 ARGs commonly associated with Acinetobacter baumannii, such as msrE, mphE (macrolide resistance), and tet(39) (tetracycline resistance). The ARGs most prevalent near the effluent pipe persisted 6.4 km downriver. Using metagenomic phylogenetic analysis (MetaPhlAn2) clade-specific marker genes, the taxa distribution near the effluent showed elevation of reads annotated as Acinetobacter species as well as gut-associated taxa, Bacteroides and Firmicutes. The ARG levels and taxa prevalence showed little dependence on seasonal chlorination of the effluent. Nitrogen and phosphorus were elevated near the effluent pipe but had no consistent correlation with ARG levels. We show that in a rural river microbiome, year-round wastewater effluent substantially elevates ARGs, including those associated with multidrug-resistant A. baumannii. IMPORTANCE Antibiotic resistance is a growing problem worldwide, with frequent transmission between pathogens and environmental organisms. Rural rivers can support high levels of recreational use by people unaware of inputs from treated wastewater, while wastewater treatment plants (WWTPs) can generate a small but significant portion of flow volume into a river surrounded by forest and agriculture. There is little information on the rural impacts of WWTP effluent on the delivery and transport of antibiotic resistance genes. In our study, the river water proximal to wastewater effluent shows evidence for the influx of multidrug-resistant Acinetobacter baumannii, an opportunistic pathogen of concern for hospitals but also widespread in natural environments. Our work highlights the importance of wastewater effluent in management of environmental antibiotic resistance, even in high quality, rural river systems.

Project description:A collection of 313 motile aeromonads isolated at Danish rainbow trout farms was analyzed to identify some of the genes involved in high levels of antimicrobial resistance found in a previous field trial (A. S. Schmidt, M. S. Bruun, I. Dalsgaard, K. Pedersen, and J. L. Larsen, Appl. Environ. Microbiol. 66:4908-4915, 2000), the predominant resistance phenotype (37%) being a combined oxytetracycline (OTC) and sulphadiazine/trimethoprim resistance. Combined sulphonamide/trimethoprim resistance (135 isolates) appeared closely related to the presence of a class 1 integron (141 strains). Among the isolates containing integrons, four different combinations of integrated resistance gene cassettes occurred, in all cases including a dihydrofolate reductase gene and a downstream aminoglycoside resistance insert (87 isolates) and occasionally an additional chloramphenicol resistance gene cassette (31 isolates). In addition, 23 isolates had "empty" integrons without inserted gene cassettes. As far as OTC resistance was concerned, only 66 (30%) out of 216 resistant aeromonads could be assigned to resistance determinant class A (19 isolates), D (n = 6), or E (n = 39); three isolates contained two tetracycline resistance determinants (AD, AE, and DE). Forty OTC-resistant isolates containing large plasmids were selected as donors in a conjugation assay, 27 of which also contained a class 1 integron. Out of 17 successful R-plasmid transfers to Escherichia coli recipients, the respective integrons were cotransferred along with the tetracycline resistance determinants in 15 matings. Transconjugants were predominantly tetA positive (10 of 17) and contained class 1 integrons with two or more inserted antibiotic resistance genes. While there appeared to be a positive correlation between conjugative R-plasmids and tetA among the OTC-resistant aeromonads, tetE and the unclassified OTC resistance genes as well as class 1 integrons were equally distributed among isolates with and without plasmids. These findings indicate the implication of other mechanisms of gene transfer besides plasmid transfer in the dissemination of antibiotic resistance among environmental motile aeromonads.

Project description:The Riverton City dump is Jamaica's largest solid waste disposal site, but it lacks engineered protection for leachate containment and treatment. Shotgun metagenomics was used to survey the microbial communities in the Riverton City dump leachate and in surface waters of the Duhaney River, an urban waterway abutting the dump. The community within the leachate pond was taxonomically distinct from that found in the surface waters of the Duhaney River. Higher microbial diversity was observed within the dump leachate, with members of the Bacteroidetes, Firmicutes, Gammaproteobacteria, Deltaproteobacteria, and Tenericutes being the most abundant, while the river community was dominated by Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria The microbial communities exhibit similar functional potential profiles, including chemoorganoheterotrophy as the dominant metabolism, and the potential to degrade aromatic compounds. From reconstruction of metagenome-assembled genomes (MAGs), organisms within both environments are predicted to survive in the presence of multiple antibiotics, antiseptics, biocides, and metals. Strong virulence potential coincided with the most diverse multiple resistance profiles in 1 of 5 leachate MAGs and 5 of 33 river MAGs. Unexpectedly, the microbial resistance profiles were more varied and widespread in the river populations, where we had expected the chemical composition of the leachate to select and enrich for resistance characteristics. This study provides valuable insights into the total functional potential of a landfill leachate microbial community and identifies possible human health hazards within the Duhaney River and Riverton City dump, urban environments with the potential to impact human populations.IMPORTANCE Landfill leachate is a persistent contamination threat for terrestrial waters. Microbial metabolism in landfills transforms contaminants and contributes to greenhouse gas emissions. A better understanding of landfill-associated microbial communities will inform bioremediation of solid waste environments and improve pathogen monitoring. We leveraged shotgun metagenomics to investigate the microbial communities of the Riverton City dump and the adjoining Duhaney River near Kingston City, Jamaica. We identified no overlap between the microbial communities inhabiting the Riverton City dump leachate and the Duhaney River. Both communities are predicted to degrade aromatic compounds, which are ubiquitous environmental pollutants. Adversely, microbes in both environments are predicted to withstand widely used antibiotics, antiseptics, and metal contamination. The absence of evidence for microbial transfer from the leachate to the river is encouraging; however, the Duhaney River contained several organisms with predicted pathogenic lifestyles, indicating that the river represents a human health risk regardless of impact from the dump.

Project description:High-throughput genomic technologies offer new approaches for environmental health monitoring, including metagenomic surveillance of antibiotic resistance determinants (ARDs). Although natural environments serve as reservoirs for antibiotic resistance genes that can be transferred to pathogenic and human commensal bacteria, monitoring of these determinants has been infrequent and incomplete. Furthermore, surveillance efforts have not been integrated into public health decision making.We used a metagenomic epidemiology-based approach to develop an ARD index that quantifies antibiotic resistance potential, and we analyzed this index for common modal patterns across environmental samples. We also explored how metagenomic data such as this index could be conceptually framed within an early risk management context.We analyzed 25 published data sets from shotgun pyrosequencing projects. The samples consisted of microbial community DNA collected from marine and freshwater environments across a gradient of human impact. We used principal component analysis to identify index patterns across samples.We observed significant differences in the overall index and index subcategory levels when comparing ecosystems more proximal versus distal to human impact. The selection of different sequence similarity thresholds strongly influenced the index measurements. Unique index subcategory modes distinguished the different metagenomes.Broad-scale screening of ARD potential using this index revealed utility for framing environmental health monitoring and surveillance. This approach holds promise as a screening tool for establishing baseline ARD levels that can be used to inform and prioritize decision making regarding management of ARD sources and human exposure routes.Port JA, Cullen AC, Wallace JC, Smith MN, Faustman EM. 2014. Metagenomic frameworks for monitoring antibiotic resistance in aquatic environments. Environ Health Perspect 122:222–228; http://dx.doi.org/10.1289/ehp.1307009

Project description:Contaminated sites are recognized as the "hotspot" for the development and spread of antibiotic resistance in environmental bacteria. It is very challenging to understand mechanism of development of antibiotic resistance in polluted environment in the presence of different anthropogenic pollutants. Uncertainties in the environmental processes adds complexity to the development of resistance. This study attempts to develop mathematical model by using stochastic partial differential equations for the transport of fluoroquinolone and its resistant bacteria in riverine environment. Poisson's process is assumed for the diffusion approximation in the stochastic partial differential equations (SPDE). Sensitive analysis is performed to evaluate the parameters and variables for their influence over the model outcome. Based on their sensitivity, the model parameters and variables are chosen and classified into environmental, demographic, and anthropogenic categories to investigate the sources of stochasticity. Stochastic partial differential equations are formulated for the state variables in the model. This SPDE model is then applied to the 100 km stretch of river Musi (South India) and simulations are carried out to assess the impact of stochasticity in model variables on the resistant bacteria population in sediments. By employing the stochasticity in model variables and parameters we came to know that environmental and anthropogenic variations are not able to affect the resistance dynamics at all. Demographic variations are able to affect the distribution of resistant bacteria population uniformly with standard deviation between 0.087 and 0.084, however, is not significant to have any biological relevance to it. The outcome of the present study is helpful in simplifying the model for practical applications. This study is an ongoing effort to improve the model for the transport of antibiotics and transport of antibiotic resistant bacteria in polluted river. There is a wide gap between the knowledge of stochastic resistant bacterial growth dynamics and the knowledge of transport of antibiotic resistance in polluted aquatic environment, this study is one step towards filling up that gap.

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Dataset Information

A simple model of tetracycline antibiotic resistance in the aquatic environment (with application to the Poudre River).

Publications

A simple model of tetracycline antibiotic resistance in the aquatic environment (with application to the Poudre River).

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