Skip to main content
SpringerLink
Log in

Molecular Ecology Of Macrolide–Lincosamide–Streptogramin B Methylases in Waste Lagoons and Subsurface Waters Associated with Swine Production

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

RNA methylase genes are common antibiotic resistance determinants for multiple drugs of the macrolide, lincosamide, and streptogramin B (MLSB) families. We used molecular methods to investigate the diversity, distribution, and abundance of MLSB methylases in waste lagoons and groundwater wells at two swine farms with a history of tylosin (a macrolide antibiotic structurally related to erythromycin) and tetracycline usage. Phylogenetic analysis guided primer design for quantification of MLSB resistance genes found in tylosin-producing Streptomyces (tlr(B), tlr(D)) and commensal/pathogenic bacteria (erm(A), erm(B), erm(C), erm(F), erm(G), erm(Q)). The near absence of tlr genes at these sites suggested a lack of native antibiotic-producing organisms. The gene combination erm(ABCF) was found in all lagoon samples analyzed. These four genes were also detected with high frequency in wells previously found to be contaminated by lagoon leakage. A weak correlation was found between the distribution of erm genes and previously reported patterns of tetracycline resistance determinants, suggesting that dissemination of these genes into the environment is not necessarily linked. Considerations of gene origins in history (i.e., phylogeny) and gene distributions in the landscape provide a useful “molecular ecology” framework for studying environmental spread of antibiotic resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Aminov RI, Chee-Sanford JC, Garrigues N, Teferedegne B, Krapac IJ, White BA, Mackie RI (2002) Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microbiol 68:1786–1793

    Article  CAS  PubMed  Google Scholar 

  2. Aminov RI, Garrigues-Jeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32

    Article  CAS  PubMed  Google Scholar 

  3. Aminov RI, Mackie RI (2007) Evolution and ecology of antibiotic resistance genes. FEMS Microbiol Lett 271:147–161

    Article  CAS  PubMed  Google Scholar 

  4. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BFF, Rapp BA, Wheeler DL (1999) GenBank. Nucleic Acids Res 27:12–17

    Article  CAS  PubMed  Google Scholar 

  5. Berrang ME, Ladely SR, Meinersmann RJ, Fedorka-Cray PJ (2007) Subtherapeutic tylosin phosphate in broiler feed affects Campylobacter on carcasses during processing. Poultry Sci 86:1229–1233

    CAS  Google Scholar 

  6. Berryman DI, Lyristis M, Rood JI (1994) Cloning and sequence analysis of ermQ, the predominant macrolide-lincosamide-streptogramin B resistance gene in Clostridium perfringens. Antimicrob Agents Chemother 38:1041–1046

    CAS  PubMed  Google Scholar 

  7. Bryskier AJ, Butzler JP, Neu HC, Tulkens PM (1993) Macrolides: chemistry, pharmacology, and clinical uses. Arnette Blackwell, Paris

    Google Scholar 

  8. 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 67:1494–1502

    Article  CAS  PubMed  Google Scholar 

  9. Chee-Sanford JC, Mackie RI, Koike S, Krapac I, Lin Y-F, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108

    Article  CAS  PubMed  Google Scholar 

  10. Chen J, Fluharty FL, St-Pierre N, Morrison M, Yu Z (2008) Technical note: occurrence in fecal microbiota of genes conferring resistance to both macrolide–lincosamide–streptogramin B and tetracyclines concomitant with feeding of beef cattle with tylosin. J Anim Sci 86:2385–2391

    Article  CAS  PubMed  Google Scholar 

  11. Chen J, Yu ZT, Michel FC, Wittum T, Morrison M (2007) Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides–lincosamides–streptogramin B in livestock manure and manure management systems. Appl Environ Microbiol 73:4407–4416

    Article  CAS  PubMed  Google Scholar 

  12. Cooper AJ, Shoemaker NB, Salyers AA (1996) Erythromycin resistance gene from the Bacteroides conjugal transposon Tcr Ermr 7853 is nearly identical to ermG from Bacillus sphaericus. Antimicrob Agents Chemother 40:506–508

    CAS  PubMed  Google Scholar 

  13. D'Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377

    Article  PubMed  Google Scholar 

  14. De Graef EM, Decostere A, De Leener E, Goossens H, Baele M, Haesebrouck F (2007) Prevalence and mechanism of resistance against macrolides, lincosamides, and streptogramins among Enterococcus faecium isolates from food-producing animals and hospital patients in Belgium. Microb Drug Resist 13:135–141

    Article  PubMed  Google Scholar 

  15. De Leener E, Decostere A, De Graef EM, Moyaert H, Haesebrouck F (2005) Presence and mechanism of antimicrobial resistance among enterococci from cats and dogs. Microb Drug Resist 11:395–403

    Article  PubMed  Google Scholar 

  16. De Leener E, Martel A, Decostere A, Haesebrouck F (2004) Distribution of the erm(B) gene, tetracycline resistance genes, and TN1545-like transposons in macrolide- and lincosamide-resistant enterococci from pigs and humans. Microb Drug Resist Mechan Epidemiol Dis 10:341–345

    Google Scholar 

  17. Heuer H, Krogerrecklenfort E, Wellington EMH, Egan S, van Elsas JD, van Overbeek L, Collard JM, 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 

  18. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  19. Jindal A, Kocherginskaya S, Mehboob A, Robert M, Mackie RI, Raskin L, Zilles JL (2006) Antimicrobial use and resistance in swine waste treatment systems. Appl Environ Microbiol 72:7813–7820

    Article  CAS  PubMed  Google Scholar 

  20. Jost BH, Trinh HT, Songer JG, Billington SJ (2004) A second tylosin resistance determinant, Erm B, in Arcanobacterium pyogenes. Antimicrob Agents Chemother 48:721–727

    Article  CAS  PubMed  Google Scholar 

  21. Koike S, Krapac IG, Oliver HD, Yannarell AC, Chee-Sanford JC, Aminov RI, Mackie RI (2007) Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities. Appl Environ Microbiol 73:4813–4823

    Article  CAS  PubMed  Google Scholar 

  22. Krapac I, Dey WS, Smyth CA, Roy WR (1998) Impacts of bacteria, metals, and nutrients on groundwater at two hog confinement facilities. In: Proceedings of Animal feeding operations on groundwater: issues, impact, and solutions: a conference for the future. National Ground Water Association, St. Louis, MO, pp. 29–50

  23. Krapac IG, Koike S, Meyer MT, Snow DD, Chou SFJ, Mackie RI, Roy WR, Chee-Sanford JC (2004) Long-term monitoring of the occurrence of antibiotic resistance genes in groundwater near swine confinement facilities. Proceedings of the 4th International conference on pharmaceuticals and endocrine disrupting chemicals in water. National Ground Water Association, Minneapolis, MN, pp. 158–172

  24. Ladely SR, Harrison MA, Fedorka-Cray PJ, Berrang ME, Englen MD, Meinersmann RJ (2007) Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. J Food Prot 70:1945–1951

    PubMed  Google Scholar 

  25. Larson TH, Krapac IG, Dey WS, Suchomski CJ (1997) Electromagnetic terrain conductivity surveys used to screen swine confinement facilities for groundwater contamination. Presented at the Proceedings of the symposium on the application of geophysics to engineering and environmental problems, Reno, NV

  26. Legendre P, Legendre L (1998) Numerical ecology, second English ed. Elsevier, Amsterdam

    Google Scholar 

  27. Liu MF, Kirpekar F, van Wezel GP, Douthwaite S (2000) The tylosin resistance gene tlrB of Streptomyces fradiae encodes a methyltransferase that targets G748 in 23S rRNA. Mol Microbiol 37:811–820

    Article  CAS  PubMed  Google Scholar 

  28. Mackie RI, Koike S, Krapac I, Chee-Sanford J, Maxwell S, Aminov RI (2006) Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities. Anim Biotechnol 17:157–176

    Article  CAS  PubMed  Google Scholar 

  29. McEwen SA (2006) Antibiotic use in animal agriculture: what have we learned and where are we going? Anim Biotechnol 17:239–250

    Article  PubMed  Google Scholar 

  30. Miller DN (2001) Evaluation of gel filtration resins for the removal of PCR-inhibitory substances from soils and sediments. J Microbiol Methods 44:49–58

    Article  CAS  PubMed  Google Scholar 

  31. Portillo A, Ruiz-Larrea F, Zarazaga M, Alonso A, Martinez JL, Torres C (2000) Macrolide resistance genes in Enterococcus spp. Antimicrob Agents Chemother 44:967–971

    Article  CAS  PubMed  Google Scholar 

  32. R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  33. Rasmussen JL, Odelson DA, Macrina FL (1986) Complete nucleotide sequence and transcription of ermF, a macrolide–lincosamide–streptogramin B resistance determinant from Bacteroides fragilis. J Bacteriol 168:523–533

    CAS  PubMed  Google Scholar 

  34. Roberts MC (2002) Resistance to tetracycline, macrolide-lincosamide-streptogramin, trimethoprim, and sulfonamide drug classes. Mol Biotechnol 20:261–283

    Article  CAS  PubMed  Google Scholar 

  35. Roberts MC (2008) Update on macrolide–lincosamide–streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147–159

    Article  CAS  PubMed  Google Scholar 

  36. Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999) Nomenclature for macrolide and macrolide–lincosamide–streptogramin B resistance determinants. Antimicrob Agents Chemother 43:2823–2830

    CAS  PubMed  Google Scholar 

  37. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  38. Salyers A, Shoemaker NB (2006) Reservoirs of antibiotic resistance genes. Anim Biotechnol 17:137–146

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  40. Sutcliffe J, Grebe T, TaitKamradt A, Wondrack L (1996) Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40:2562–2566

    CAS  PubMed  Google Scholar 

  41. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  42. Tsai YL, Olson BH (1991) Rapid method for direct extraction of DNA from soil and sediments. Appl Environ Microbiol 57:1070–1074

    CAS  PubMed  Google Scholar 

  43. Wegener HC (2003) Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol 6:439–445

    Article  CAS  PubMed  Google Scholar 

  44. Witte W (2000) Ecological impact of antibiotic use in animals on different complex microflora: environment. Int J Antimicrob Agents 14:321–325

    Article  CAS  PubMed  Google Scholar 

  45. Yu ZT, Michel FC, Hansen G, Wittum T, Morrison M (2005) Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl Environ Microbiol 71:6926–6933

    Article  CAS  PubMed  Google Scholar 

  46. Zhou JZ, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by funding from the USDA NRI Competitive Grants Program 26.0 (award nos. 2001-35102-10774 and 2005-35102-16424). Support was also provided by the Scottish Government Rural and Environmental Research and Analysis Directorate and by Hatch funding to the Agricultural Experimental Station at the University of Illinois at Urbana-Champaign.

Author information

Author notes

  1. Satoshi Koike

    Present address: Research Faculty of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan

Authors and Affiliations

  1. Department of Animal Sciences, University of Illinois at Urbana-Champaign, 1207 W. Gregory Dr., Urbana, IL, 61801, USA

    Satoshi Koike, A. C. Yannarell, Holly D. Gans & Roderick I. Mackie

  2. Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK

    Rustam I. Aminov

  3. Illinois State Geological Survey, Champaign, IL, 61820, USA

    Ivan G. Krapac

  4. USDA Agricultural Research Service, Urbana, IL, 61801, USA

    Joanne C. Chee-Sanford

  5. Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    A. C. Yannarell & Roderick I. Mackie

Authors
  1. Satoshi Koike
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rustam I. Aminov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. C. Yannarell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Holly D. Gans
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ivan G. Krapac
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joanne C. Chee-Sanford
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Roderick I. Mackie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roderick I. Mackie.

Additional information

S. Koike, R. I. Aminov, and A. C. Yannarell contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koike, S., Aminov, R.I., Yannarell, A.C. et al. Molecular Ecology Of Macrolide–Lincosamide–Streptogramin B Methylases in Waste Lagoons and Subsurface Waters Associated with Swine Production. Microb Ecol 59, 487–498 (2010). https://doi.org/10.1007/s00248-009-9610-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-009-9610-0

Keywords

Search

Navigation