Abstract

Fifteen soil and 45 vegetable samples from Detroit community gardens were analyzed for potential antimicrobial resistance contamination. Soil bacteria were isolated and tested by antimicrobial susceptibility profiling, horizontal gene transfer, and whole-genome sequencing. High-throughput 16S rRNA sequencing analysis was conducted on collected soil samples to determine the total bacterial composition. Of 226 bacterial isolates recovered, 54 were from soil and 172 from vegetables. A high minimal inhibitory concentration (MIC) was defined as the MIC greater than or equal to the resistance breakpoint of Escherichia coli for Gram-negative bacteria or Staphylococcus aureus for Gram-positive bacteria. The high MIC was observed in 63.4 and 69.8% of Gram-negative isolates from soil and vegetables, respectively, against amoxicillin/clavulanic acid, as well as 97.5 and 82.7% against ampicillin, 97.6 and 90.7% against ceftriaxone, 85.4 and 81.3% against cefoxitin, 65.8 and 70.5% against chloramphenicol, and 80.5 and 59.7% against ciprofloxacin. All Gram-positive bacteria showed a high MIC to gentamicin, kanamycin, and penicillin. Forty of 57 isolates carrying tetM (70.2%) successfully transferred tetracycline resistance to a susceptible recipient via conjugation. Whole-genome sequencing analysis identified a wide array of antimicrobial resistance genes (ARGs), including those encoding AdeIJK, Mex, and SmeDEF efflux pumps, suggesting a high potential of the isolates to become antimicrobial resistant, despite some inconsistency between the gene profile and the resistance phenotype. In conclusion, soil bacteria in urban community gardens can serve as a reservoir of antimicrobial resistance with the potential to transfer to clinically important pathogens, resulting in food safety and public health concerns.

Highlights

  • The environmental reservoir of antimicrobial resistance has drawn extensive research attention due to their connection with antimicrobial resistance in human pathogens (Hu et al, 2018; Kraemer et al, 2019; Zhang et al, 2019b; Scott et al, 2020)

  • A diverse collection of soil bacteria recovered from Detroit urban community gardens demonstrated a high minimal inhibitory concentration (MIC) to a wide range of antibiotics, including those of clinical significance

  • Added to the significance was the successful conjugation of antimicrobial resistance to a susceptible E. coli or Enterococcus faecalis recipient, underlying that soil bacteria could transfer antimicrobial resistance to foodborne pathogens and pose a public health concern

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Summary

Introduction

The environmental reservoir of antimicrobial resistance has drawn extensive research attention due to their connection with antimicrobial resistance in human pathogens (Hu et al, 2018; Kraemer et al, 2019; Zhang et al, 2019b; Scott et al, 2020). The high DNA sequence similarity of environmental antimicrobial resistance genes (ARGs) with human pathogens (Forsberg et al, 2012) and fecal microorganisms (Nesme et al, 2014) suggests a common pool of ARG between human and the environment. Multidrug-resistant bacteria of diverse genera have been found in urban, agricultural, and pristine soils (Walsh and Duffy, 2013), the food safety implication of the potential of soil bacteria in disseminating ARGs remains under investigated. Peri-urban arable soils demonstrated more diverse and abundant ARGs compared to peri-urban pristine soil, implicating possible food safety concern associated with vegetables grown in these soils (Xiang et al, 2018). Another study recovered E. coli and Enterococcus from vegetables grown in urban gardens and found that more than 60% of E. coli were ampicillin resistant as well as 86.8% of Enterococcal isolates resistant to ampicillin, ciprofloxacin, erythromycin, streptomycin, and tetracycline (Perera et al, 2020)

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