Air-drying beds reduce the quantities of antibiotic resistance genes and class 1 integrons in residual municipal wastewater solids

Environmental Science and Technology

Volumn 47, Issue 17, 2013, Pages 9965-9971

  Burch, Tucker R ^a   Sadowsky, Michael J ^a   Lapara, Timothy M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE GENES; CLASS 1 INTEGRONS; MICROBIAL COMMUNITIES; MUNICIPAL WASTEWATERS; OPERATING PRACTICES; ORDERS OF MAGNITUDE; RESISTANCE MECHANISMS; TARGET CONCENTRATIONS;

GENES; POLYMERASE CHAIN REACTION; RNA;

SOLAR DRYERS;

INTEGRASE; RNA 16S;

ANTIBIOTICS; BACTERIUM; CONCENTRATION (COMPOSITION); GENE EXPRESSION; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; WASTEWATER;

AIR DRYING BED; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BIOTECHNOLOGICAL PROCEDURES; CONCENTRATION (PARAMETERS); GENE TARGETING; HALF LIFE TIME; INTEGRON; MICROBIAL COMMUNITY; MUNICIPAL SOLID WASTE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PROTEINS; DRUG RESISTANCE, MICROBIAL; INTEGRONS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; WASTE DISPOSAL, FLUID; WASTE WATER; WATER POLLUTANTS, CHEMICAL; WATER POLLUTION, CHEMICAL;

EID: 84883532158     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es4024749     Document Type: Article

References (41)

1. Levy, S. B. The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Powers; 2 nd ed.; Perseus Books Group: Cambridge, MA, 2002.
2. Levy, S. B.; Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses Nat. Med. 2004, 10, S122-S129
3. Pruden, A.; Pei, R.; Storteboom, H.; Carlson, K. H. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado Environ. Sci. Technol. 2006, 40, 7445-7450
4. Auerbach, E. A.; Seyfried, E. E.; McMahon, K. D. Tetracycline resistance genes in activated sludge wastewater treatment plants Water Res. 2007, 41, 1143-1151
5. Börjesson, S.; Dienues, O.; Jarnheimer, P.-A.; Olsen, B.; Matussek, A.; Lindgren, P.-E. Quantification of genes encoding resistance to aminoglycosides, β-lactams and tetracyclines in wastewater environments by real-time PCR Int. J. Environ. Health Res. 2009, 19, 219-230
6. Börjesson, S.; Melin, S.; Matussek, A.; Lindgren, P.-E. A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-resistant S. aureus in a municipal wastewater treatment plant Water Res. 2009, 43, 925-932
7. Ghosh, S.; Ramsden, S. J.; LaPara, T. M. The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants Appl. Microbiol. Biotechnol. 2009, 84, 791-796
8. Kim, S.; Park, H.; Chandran, K. Propensity of activated sludge to amplify or attenuate tetracycline resistance genes and tetracycline resistant bacteria: a mathematical modeling approach Chemosphere 2010, 78, 1071-1077
9. TEM) genes in a wastewater stream Appl. Environ. Microbiol. 2009, 75, 203-211
10. LaPara, T. M.; Burch, T. R.; McNamara, P. J.; Tan, D. T.; Yan, M.; Eichmiller, J. J. Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior Harbor Environ. Sci. Technol. 2011, 45, 9543-9549
11. Munir, M.; Wong, K.; Xagoraraki, I. Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan Water Res. 2011, 45, 681-693
12. Uyaguari, M. I.; Fichot, E. B.; Scott, G. I.; Norman, R. S. Characterization and quantitation of a novel β-lactamase gene within a wastewater treatment facility and surrounding coastal ecosystem Appl. Environ. Microbiol. 2011, 77, 8226-8233
13. Volkmann, H.; Schwartz, T.; Bischoff, P.; Kirchen, S.; Obst, U. Detection of clinically relevant antibiotic-resistance genes in municipal wastewater using real-time PCR (TaqMan) J. Microbiol. Methods 2004, 56, 277-286
14. Zhang, X.-X.; Zhang, T. Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations Environ. Sci. Technol. 2011, 45, 2598-2604
15. Zhang, T.; Zhang, M.; Zhang, X.; Fang, H. H. Tetracycline resistance genes and tetracycline resistant Enterobacteriaceae in activated sludge of sewage treatment plants Environ. Sci. Technol. 2009, 43, 3455-3460
16. Zhang, X.-X.; Zhang, T.; Zhang, M.; Fang, H. H. P.; Cheng, S.-P. Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants Appl. Microbiol. Biotechnol. 2009, 82, 1169-1177
17. Ma, Y.; Wilson, C. A.; Novak, J. T.; Riffat, R.; Aynur, S.; Murthy, S.; Pruden, A. Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons Environ. Sci. Technol. 2011, 45, 7855-7861
18. Diehl, D. L.; LaPara, T. M. Effect of temperature on the fate of genes encoding tetracycline resistance and the integrase of class 1 integrons within anaerobic and aerobic digesters treating municipal wastewater solids Environ. Sci. Technol. 2010, 44, 9128-9133
19. Beecher, N.; Crawford, K.; Goldstein, N.; Kester, G.; Lono-Batura, M.; Dziezyk, E.; Peckenham, J.; Cheng, T. Final Report: A National Biosolids Regulation, Quality, End Use, & Disposal Survey; North East Biosolids and Residuals Association: Tamworth, NH, 2007.
20. Standards for the Use or Disposal of Sewage Sludge. Code of Federal Regulations, Part 503, Title 40, 2007.
21. Tchobanoglous, G.; Burton, F. L.; Stensel, H. D. Wastewater Engineering: Treatment and Reuse, 4 th ed.; McGraw-Hill: Boston, MA, 2003.
22. Aminov, R. I.; Garrigues-Jeanjean, N.; Mackie, R. I. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection Appl. Environ. Microbiol. 2001, 67, 22-32
23. Chen, J.; Yu, Z.; Michel, F. C.; Wittum, T.; Morrison, M. 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. 2007, 73, 4407-4416
24. Goldstein, C.; Lee, M. D.; Sanchez, S.; Hudson, C.; Phillips, B.; Register, B.; Grady, M.; Liebert, C.; Summers, A. O.; White, D. G.; Maurer, J. J. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics Antimicrob. Agents Chemother. 2001, 45, 723-726
25. Heuer, H.; Smalla, K. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months Environ. Microbiol. 2007, 9, 657-666
26. Ng, L.-K.; Martin, I.; Alfa, M.; Mulvey, M. Multiplex PCR for the detection of tetracycline resistant genes Mol. Cell. Probes 2001, 15, 209-215
27. Levy, S. B.; McMurry, L. M.; Barbosa, T. M.; Burdett, V.; Courvalin, P.; Hillen, W.; Roberts, M. C.; Rood, J. I.; Taylor, D. E. Nomenclature for new tetracycline resistance determinants Antimicrob. Agents Chemother. 1999, 43, 1523-1524
28. Roberts, M. C.; Sutcliffe, J.; Courvalin, P.; Jensen, L. B.; Rood, J.; Seppala, H. Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants Antimicrob. Agents Chemother. 1999, 43, 2823-2830
29. Mazel, D. Integrons: agents of bacterial evolution Nat. Rev. Microbiol. 2006, 4, 608-620
30. Bernhard, A. E.; Field, K. G. A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA Appl. Environ. Microbiol. 2000, 66, 4571-4574
31. Layton, A.; McKay, L.; Williams, D.; Garrett, V.; Gentry, R.; Sayler, G. Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water Appl. Environ. Microbiol. 2006, 72, 4214-4224
32. Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA Appl. Environ. Microbiol. 1993, 59, 695-700
33. Seurinck, S.; Defoirdt, T.; Verstraete, W.; Siciliano, S. D. Detection and quantification of the human-specific HF183 Bacteroides 16S rRNA genetic marker with real-time PCR for assessment of human faecal pollution in freshwater Environ. Microbiol. 2005, 7, 249-259
34. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular Cloning: A Laboratory Manual, 2 nd ed.; Coldspring Harbor Laboratory: Coldspring Harbor, NY, 1989.
35. Engemann, C. A.; Keen, P. L.; Knapp, C. W.; Hall, K. J.; Graham, D. W. Fate of tetracycline resistance genes in aquatic systems: migration from the water column to peripheral biofilms Environ. Sci. Technol. 2008, 42, 5131-5136
36. Zhang, W.; Sturm, B. S. M.; Knapp, C. W.; Graham, D. W. Accumulation of tetracycline resistance genes in aquatic biofilms due to periodic waste loadings from swine lagoons Environ. Sci. Technol. 2009, 43, 7643-7650
37. Burch, T. R.; Sadowsky, M. J.; LaPara, T. M. Aerobic digestion reduces the quantity of antibiotic resistance genes in residual municipal wastewater solids. Front. Microbiol. [Online] 2013, 4, Article 17. http://www.frontiersin. org/Antimicrobials,-Resistance-and-Chemotherapy/10.3389/fmicb.2013.00017/ abstract (accessed Feb 18, 2013).
38. Cook, R. D.; Weisberg, S. Applied Regression Including Computing and Graphics; John Wiley & Sons: Hoboken, NJ, 1999.
39. Engemann, C. A.; Adams, L.; Knapp, C. W.; Graham, D. W. Disappearance of oxytetracycline resistance genes in aquatic systems FEMS Microbiol. Lett. 2006, 263, 176-182
40. Rogers, S. W.; Donnelly, M.; Peed, L.; Kelty, C. A.; Mondal, S.; Zhong, Z.; Shanks, O. C. Decay of bacterial pathogens, fecal indicators, and real-time quantitative PCR genetic markers in manure-amended soils Appl. Environ. Microbiol. 2011, 77, 4839-4848
41. Stalder, T.; Barraud, O.; Casellas, M.; Dagot, C.; Ploy, M.-C. Integron involvement in environmental spread of antibiotic resistance. Front. Microbiol. [Online] 2012, 3, Article 119. http://www.frontiersin.org/Antimicrobials,- Resistance-and-Chemotherapy/10.3389/fmicb.2012.00119/abstract (accessed Nov 20, 2012).