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Patterns of Multi-Antibiotic-Resistant Escherichia Coli from Streams with No History of Antimicrobial Inputs

Microbial Ecology volume 72, pages 840–850 (2016)Cite this article

Abstract

A growing body of evidence suggests that contaminated environments may harbor a greater proportion of antibiotic-resistant microorganisms than unpolluted reference sites. Here, we report the screening of 427 Escherichia coli strains isolated from 11 locations on nine streams draining the US Department of Energy’s Savannah River Site against a panel of five antibiotics. Streams were chosen to capture a wide range of watersheds from minimally disturbed to highly impacted. Overall, higher levels of resistance were found in waterborne E. coli that also generally exhibited low spatial variability. However, 3 of 11 locations also demonstrated elevated resistance levels in sediments. Two of these occurred in highly disturbed tributaries with no obvious sources of antimicrobials. To further investigate these patterns, we screened a subset of isolates obtained from three streams against 23 antibiotics or antibiotic combinations. A large proportion of these isolates (>40 %) demonstrated resistance to 10 or more antimicrobials, suggesting that environmental multi-antibiotic resistance may be prevalent in this bacterial commensal. Only 4 of 87 viable isolates were tested susceptible to all 23 antibiotics and combinations. Among these multi-antibiotic-resistant isolates, several demonstrated resistance to all structural classes of antimicrobial agents tested, including frontline antibiotics such as gatifloxacin and ciprofloxacin.

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References

  1. Allen SE, Boerlin P, Janecko N, Lumsden JS, Barker IK, Pearl DL, Reid-Smith RJ, Jardine C (2011) Antimicrobial resistance in Generic Escherichia coli isolates from wild small mammals living in swine farm, residential, landfill and natural environments in Southern Ontario, Canada. Appl Environ Microbiol 77:882–888

    Article  CAS  PubMed  Google Scholar 

  2. Auer MT, Niehaus SL (1993) Modeling fecal coliform bacteria—1. Field and laboratory determination of loss kinetics. Water Res 27:693–701

    Article  Google Scholar 

  3. Bai S, Lung W (2005) Modeling sediment impact on the transport of fecal bacteria. Water Res 39:5232–5240

    Article  CAS  PubMed  Google Scholar 

  4. Baker-Austin C, McArthur JV, Lindell AH, Wright MS, Tuckfield RC, Gooch J, Warne L, Oliver J, Stepanauskas R (2007) Multi-site analysis reveals widespread antibiotic resistance in the marine pathogen vibrio vulnificus. Microb Ecol 57:151–159

    Article  Google Scholar 

  5. Baker-Austin C, McArthur JV, Tuckfield RC, Najarro M, Lindell AH, Gooch J, Stepanauskas R (2008) Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia dn South Carolina, USA. J Food Prot 71:2552–2558

    CAS  PubMed  Google Scholar 

  6. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  CAS  PubMed  Google Scholar 

  7. Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI (2001) Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying Two swine production facilities. Appl Environ Microbiol 57:1494–1502

    Article  Google Scholar 

  8. D’Costa VM, McGrann KM, Hughes DH, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377

    Article  PubMed  Google Scholar 

  9. D’Costa VM, Griffiths E, Wright GD (2007) Expanding the soil resistome: exploring environmental diversity. Curr Opin Microbiol 10:481–489

    Article  PubMed  Google Scholar 

  10. Dang H, Ren J, Sosng L, Sun S, An L (2008) Diverse tetracycline resistant bacteria and resistance genes from coastal waters of jiaozhou Bay. Microb Ecol 55:237–246

    Article  CAS  PubMed  Google Scholar 

  11. Drudge CN, Elliott AVC, Plach JM, Ejim LJ, Wright GD, Droppo IG, Warren A (2012) Diversity of integron- and culture-associated antibiotic resistance gene in freshwater floc. Appl Environ Microbiol 78:4367–4372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Enne VI, Delsol AA, Davis GR, Hayward SL, Roe JM, Bennett PM (2005) Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element. J Antimicrob Chemother 56:544–551

    Article  CAS  PubMed  Google Scholar 

  13. Enne VI, Livermore DM, Stephens P, Hall LMC (2007) Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 357:1325–1328

    Article  Google Scholar 

  14. Fletcher DE, Lindell AH, Stillings GK, Mills GL, Blas SA, McArthur JV (2014) Spatial and taxonomic variation in trace element bioaccumulation in two herbivores from a coal combustion waste contaminated stream. Ecotox Environ Safety 101:196–204

    Article  CAS  Google Scholar 

  15. Gannon JJ, Busse MK, Schillinger JE (1983) Fecal coliform disappearance in a river impoundment. Water Res 17:1595–1601

    Article  Google Scholar 

  16. Gilliver MA, Bennett M, Begon M, Hazel SM, Hart CA (1999) Antibiotic resistance found in wild rodents. Nature 401:233–234

    Article  CAS  PubMed  Google Scholar 

  17. Guardabassi L, Agersø Y (2006) Genes homologous to glycopeptide resistance vanA are widespread in soil microbial communities. FEMS Microbiol Lett 259:221–225

    Article  CAS  PubMed  Google Scholar 

  18. Heuer H, Krögerrecklenfort E, Wellington EMH, Egan S, van Elsas JD, van Overbeek L, Collard J-M, Guillaume G, Karagouni AD, Nikolakopoulou TL, Smalla K (2002) Gentamicin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol Ecol 42:289–302

    Article  CAS  PubMed  Google Scholar 

  19. Jamieson RC, Joy DM, Leeb H, Kostaschuk R, Gordon RJ (2005) Resuspension of sediment-associated Escherichia coli in a natural stream. J Environ Qual 34:581–589

    Article  CAS  PubMed  Google Scholar 

  20. Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York

    Google Scholar 

  21. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:S122–S129

    Article  CAS  PubMed  Google Scholar 

  22. Livermore DM, Warner M, Hall LMC, Enne VI, Projan SJ, Dunman PM, Wooster SL, Harrison G (2001) Antibiotic resistance in bacteria from magpies (Pica pica) and rabbits (Oryctolagus cuniculus) from west wales. Environ Microbiol 3:658–661

    Article  CAS  PubMed  Google Scholar 

  23. Mahler BJ, Personné J–C, Lods GF, Drogue C (2000) Transport of free and particulate-associated bacteria in karst. J Hydrology 238:179–193

    Article  Google Scholar 

  24. Mast MA, Turk JT (1999) Environmental characteristics and water quality of hydrologic benchmark network stations in the Eastern United States, 1963–95:U.S. Geological Survey Circular 1173–A, 158 p

  25. McArthur JV, Tuckfield RC (2000) Spatial patterns in antibiotic resistance among stream bacteria: effects of industrial pollution. Appl Environ Microbiol 66:3722–3728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Neter J, Kutner M, Wasserman W, Nachtscheim C (1996) Applied linear statistical models 4th Edition. McGraw-Hill/Irwin

  27. Perry JA, Wright GD (2013) The antibiotic resistance “mobilome”: searching for the link between environment and clinic. Front Microbiol 4:1–7

    Article  Google Scholar 

  28. Projan SJ (2003) Why is big Pharma getting out of antibacterial drug discovery? Curr Opin Microbiol 6:427–430

    Article  PubMed  Google Scholar 

  29. Projan SJ, Shlaes DM (2004) Antibacterial drug discovery: is it all downhill from here? Clin Microbiol Infect 10:18–22

    Article  PubMed  Google Scholar 

  30. Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40:7445–7450

    Article  CAS  PubMed  Google Scholar 

  31. Rencher AC, Christensen WF (2012) Methods of multivariate analysis, 3rd edn. John Wiley & Sons, NY

    Book  Google Scholar 

  32. Riesenfeld CS, Schloss PD, Handelsman J (2004) METAGENOMICS: genomic analysis of microbial communities. Annu Rev Genet 38:525–552

    Article  CAS  PubMed  Google Scholar 

  33. Rysz M, Alvarez PJJ (2004) Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Res 38:3705–3712

    Article  CAS  PubMed  Google Scholar 

  34. Schillinger JE, Gannon JJ (1985) Bacterial adsorption and suspended particles in urban storm water. Res J Water Pollut C 57:384–389

    CAS  Google Scholar 

  35. Schmidt H, Stoob K, Hamscher G, Smit E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51:267–276

    Article  Google Scholar 

  36. Shlaes DM, Sahm D, Opiela C, Spellberg B (2013) The FDA reboot of antibiotic development. Antimicrob Agents Chemother 57:4605–4607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Singer RS, Ward MF, Maldonado G (2006) Can landscape ecology untangle the complexity of antibiotic resistance? Nature Rev Microbiol 4:943–952

    Article  CAS  Google Scholar 

  38. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, McArthur JV (2005) Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environ Sci Technol 39:3671–3678

    Article  CAS  PubMed  Google Scholar 

  39. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514

    Article  CAS  PubMed  Google Scholar 

  40. Tacão M, Correia A, Henriques I (2012) Resistance to broad-spectrum antibiotics in aquatic systems: anthropogenic activities modulate the dissemination of bla CTX-M-like genes. Appl Environ Microbiol 78:4134–4140

    Article  PubMed  PubMed Central  Google Scholar 

  41. Taylor NGH, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilizing antimicrobial resistance? Trends Ecol Evol 26:278–284

    Article  PubMed  Google Scholar 

  42. Tolba S, Egan S, Kallifidas DE, Wellington MH (2002) Distribution of streptomycin resistance and biosynthesis genes in streptomycetes recovered from different soil sites. FEMS Microbiol Ecol 42:269–276

    Article  CAS  PubMed  Google Scholar 

  43. USEPA (1998) Standard methods for the examination of water and wastewater. Section 9222 D

  44. Varlik B (2013) Total maximum daily load document Times Branch SV-324 and Upper Three Runs SV-325: Escherichia coli bacteria, indicator for pathogens. Technical Report Number: 1210-13. SCDHEC

  45. Voelz NJ, McArthur JV (2000) An exploration of factors influencing lotic insect species richness. Biodivers Conserv 9:1543–1570

    Article  Google Scholar 

  46. Walsh F (2013) Investigating antibiotic resistance in non-clinical environments. Front Microbiol 4:1–5

    CAS  Google Scholar 

  47. Webster LF, Thompson BC, Fulton MH, Chestnut DE, Van Dolah RF, Leight AK, Scott GI (2004) Identification of sources of Escherichia coli in South Carolina estuaries using antibiotic resistance analysis. J Experiment Mar Biol Ecol 28:179–195

    Article  Google Scholar 

  48. Wellington EMH, Boxall ABA, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013) The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet: Infect Dis 13:155–165

    Article  CAS  Google Scholar 

  49. Wise MG, McArthur JV, Wheat C, Shimkets LJ (1996) Temporal variation in genetic diversity and structure of a lotic population of Burkholderia (Pseudomonas) cepacia. Appl Environ Microbiol 62:1558–1562

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Wise MG, Shimkets LJ, McArthur JV (1995) Genetic structure of a lotic population of Burkolderia (Pseudomonas) cepacia. Appl Environ Microbiol 61:1791–1798

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Wright MS, Baker-Austin C, Lindell AH, Stepanauskas R, Stokes HW, McArthur JV (2008) Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. ISME J 2:417–428

    Article  CAS  PubMed  Google Scholar 

  52. Wright MS, Peltier GL, Stepanauskas R, McArthur JV (2006) Bacterial tolerances to metals and antibiotics in metal contaminated and reference streams. FEMS Microbiol Ecol 58:293–302

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Paul Stankus and Angela Lindell for technical support and advice. Financial support was provided from the US Department of Energy Financial Assistance Award no. DE-FC09-96SR18546 to the University of Georgia Research Foundation.

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Authors and Affiliations

  1. Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken, SC, 29802, USA

    J. V. McArthur & D. E. Fletcher

  2. Ecostatys, LLC, Aiken, SC, USA

    R. Cary Tuckfield

  3. Centre for Environment, Fisheries and Aquaculture Science, Weymouth, Dorset, UK

    C. Baker-Austin

Authors
  1. J. V. McArthur
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  2. D. E. Fletcher
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  3. R. Cary Tuckfield
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  4. C. Baker-Austin
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Correspondence to J. V. McArthur.

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Fig6

S1. Proportions of isolates from U4, U8, and U10 resistant to various antibiotic and antibiotic combinations excluding the cephlasporins. (GIF 239 kb)

High resolution image (TIFF 173 kb)

S2. Proportions of isolates from U4, U8, and U10 resistant to various cephalasporins. (GIF 163 kb)

High resolution image (TIFF 83 kb)

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McArthur, J.V., Fletcher, D.E., Tuckfield, R.C. et al. Patterns of Multi-Antibiotic-Resistant Escherichia Coli from Streams with No History of Antimicrobial Inputs. Microb Ecol 72, 840–850 (2016). https://doi.org/10.1007/s00248-015-0678-4

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  • DOI: https://doi.org/10.1007/s00248-015-0678-4

Keywords

  • E. coli
  • Antibiotic resistance
  • Industrial activity