Antimicrobial-Resistant Bacterial Populations and Antimicrobial Resistance Genes Obtained from Environments Impacted by Livestock and Municipal Waste

PLoS One. 2015 Jul 21;10(7):e0132586. doi: 10.1371/journal.pone.0132586. eCollection 2015.

Abstract

This study compared the populations of antimicrobial-resistant bacteria and the repertoire of antimicrobial resistance genes in four environments: effluent of three municipal wastewater treatment facilities, three cattle feedlot runoff catchment ponds, three swine waste lagoons, and two "low impact" environments (an urban lake and a relict prairie). Multiple liquid and solid samples were collected from each environment. The prevalences and concentrations of antimicrobial-resistant (AMR) Gram-negative (Escherichia coli and Salmonella enterica) and Gram-positive (enterococci) bacteria were determined from individual samples (n = 174). The prevalences of 84 antimicrobial resistance genes in metagenomic DNA isolated from samples pooled (n = 44) by collection date, location, and sample type were determined. The prevalences and concentrations of AMR E. coli and Salmonella were similar among the livestock and municipal sample sources. The levels of erythromycin-resistant enterococci were significantly higher in liquid samples from cattle catchment ponds and swine waste lagoons than in liquid samples from municipal wastewater treatment facilities, but solid samples from these environments did not differ significantly. Similarly, trimethoprim/sulfamethoxazole-resistant E. coli concentrations were significantly higher in swine liquid than in municipal liquid samples, but there was no difference in solid samples. Multivariate analysis of the distribution of antimicrobial resistance genes using principal coordinate analysis showed distinct clustering of samples with livestock (cattle and swine), low impact environment and municipal samples forming three separate clusters. The numbers of class A beta-lactamase, class C beta-lactamase, and fluoroquinolone resistance genes detected were significantly higher (P < 0.05) in municipal samples than in cattle runoff or swine lagoon samples. In conclusion, we report that AMR is a very widespread phenomenon and that similar prevalences and concentrations of antimicrobial-resistant bacteria and antimicrobial resistance genes exist in cattle, human, and swine waste streams, but a higher diversity of antimicrobial resistance genes are present in treated human waste discharged from municipal wastewater treatment plants than in livestock environments.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Cattle
  • Drug Resistance, Bacterial*
  • Enterococcus / drug effects
  • Enterococcus / genetics
  • Enterococcus / isolation & purification*
  • Escherichia coli / drug effects
  • Escherichia coli / genetics
  • Escherichia coli / isolation & purification*
  • Humans
  • Livestock / microbiology*
  • Salmonella enterica / drug effects
  • Salmonella enterica / genetics
  • Salmonella enterica / isolation & purification*
  • Swine
  • Waste Disposal, Fluid / methods
  • Waste Products / analysis*
  • Wastewater / microbiology

Substances

  • Anti-Bacterial Agents
  • Waste Products
  • Waste Water

Grants and funding

This project was funded in part by the Beef Checkoff (#58-5438-3-414; to TMA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The remainder of the funding was provided by internal project funding from United States Department of Agriculture—Agricultural Research Service, Project Number 5438-42000-014-00.