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The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants

  • Environmental Biotechnology
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Abstract

In this study, the abilities of two anaerobic digestion processes used for sewage sludge stabilization were compared for their ability to reduce the quantities of three genes that encode resistance to tetracycline (tet(A), tet(O), and tet(X)) and one gene involved with integrons (intI1). A two-stage, thermophilic/mesophilic digestion process always resulted in significant decreases in the quantities of tet(X) and intI1, less frequently in decreases of tet(O), and no net decrease in tet(A). The thermophilic stage was primarily responsible for reducing the quantities of these genes, while the subsequent mesophilic stage sometimes caused a rebound in their quantities. In contrast, a conventional anaerobic digestion process rarely caused a significant decrease in the quantities of any of these genes, with significant increases occurring more frequently. Our results demonstrate that anaerobic thermophilic treatment was more efficient in reducing quantities of genes associated with the spread of antibiotic resistance compared to mesophilic digestion.

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References

  • Aitken MD, Sobsey MD, Shehee M, Blauth KE, Hill VR, Farrell JB, Nappier SP, Walters GW, Crunk PL, van Abel N (2005) Laboratory evaluation of thermophilic-anaerobic digestion to produce class A biosolids. 2. Inactivation of pathogens and indicator organisms in a continuous flow reactor followed by batch treatment. Water Environ Res 77:3028–3036

    Article  CAS  Google Scholar 

  • Alanis AJ (2005) Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 36:697–705

    Article  Google Scholar 

  • Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • Auerbach EA, Seyfried EE, McMahon KD (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res 41:1143–1151

    Article  CAS  Google Scholar 

  • Berg G, Berman D (1980) Destruction by anaerobic mesophilic and thermophilic digestion of viruses and indicator bacteria indigenous to domestic sludges. Appl Environ Microbiol 39:361–368

    Article  CAS  Google Scholar 

  • Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260

    Article  CAS  Google Scholar 

  • Davelos AL, Kinkel LL, Samac DA (2004) Spatial variation in frequency and intensity of antibiotic interactions among Streptomycetes from prairie soil. Appl Environ Microbiol 70:1051–1058

    Article  CAS  Google Scholar 

  • Falagas ME, Bliziotis IA (2007) Pandrug-resistant gram-bacteria in an urban wastewater treatment plant. FEMS Microbiol Ecol 55:322–329

    Google Scholar 

  • Firl SJ (2006) Prevalence, fate, and characterization of antibiotic-resistant bacteria in municipal wastewater treatment plants. MS Thesis, University of Minnesota, Minneapolis, MN

  • Ghosh S (2007) Characterization of antibiotic resistance in soils exposed to manure from farms using subtherapeutic antibiotics for growth promotion. Ph. D Thesis, University of Minnesota, Minneapolis, MN

  • Grewal SK, Rajeev S, Sreevatsan S, Michel FC (2006) Persistence of Mycobacterium avium subsp. paratuberculosis and other zoonotic pathogens during simulated compositing, manure packing, and liquid storage of dairy manure. Appl Environ Microbiol 72:565–574

    Article  CAS  Google Scholar 

  • Han I, Congeevaram S, Park J (2009) Improved control of multiple-antibiotic-resistance-related microbial risk in swine manure wastes by autothermal thermophilic aerobic digestion. Water Sci Technol 59:267–271

    Article  Google Scholar 

  • Iranpour R, Cox HHJ (2006) Recurrence of fecal coliforms and Salmonella species in biosolids following thermophilic anaerobic digestion. Water Environ Res 78:1005–1012

    Article  CAS  Google Scholar 

  • Lang NL, Smith SR (2008) Time and temperature inactivation kinetics of enteric bacteria relevant to sewage sludge processes for agricultural use. Water Res 42:2229–2241

    Article  CAS  Google Scholar 

  • Livermore DM (2003) Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 26:S11–S23

    Article  Google Scholar 

  • Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608–620

    Article  CAS  Google Scholar 

  • Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Article  CAS  Google Scholar 

  • Ng L-K, Martin I, Alfa M, Mulvey MR (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Schluter A, Szczepanowski R, Pühler A, Top EM (2007) Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol Rev 31:449–477

    Article  Google Scholar 

  • Smith DL, Dushoff J, Morris JG (2005) Agricultural antibiotics and human health. PLoS Med 2:e232

    Article  Google Scholar 

  • Snyder L, Champness W (2007) Molecular genetics of bacteria, 3rd edn. ASM Press, Washington DC

    Google Scholar 

  • Summers AO (2002) Generally overlooked fundamentals of bacterial genetics and ecology. Clin Infect Dis 34:S85–S92

    Article  CAS  Google Scholar 

  • Tchobanoglous G, Burton FL, Stensel HD (2003) Wastewater engineering: treatment and reuse, 4th edn. Metcalf and Eddy, Inc, McGraw-Hill, Boston

    Google Scholar 

  • US EPA (1994) Standards for the use or disposal of sewage sludge. Code of Federal Regulations, Title 40, Chapter 503

  • Wagner AO, Gstraunthaler G, Illmer P (2008) Survival of bacterial pathogens during the thermophilic anaerobic digestion of biowaste: laboratory experiments and in situ validation. Anaerobe 14:181–183

    Article  CAS  Google Scholar 

  • Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186

    Article  CAS  Google Scholar 

  • Zhang T, Zhang M, Zhang X, Fang HHP (2009a) Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ Sci Technol 43:3455–3460

    Article  CAS  Google Scholar 

  • Zhang X, Zhang T, Zhang M, Fang HHP, Cheng S-P (2009b) Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biotechnol 82:1169–1177

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by a grant from the Center for Urban and Regional Affairs to TML and a fellowship from Geomatrix Consultants to SJR.

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Author notes

  1. Sudeshna Ghosh

    Present address: Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, MI, USA

  2. Sara J. Ramsden

    Present address: Barr Engineering, Minneapolis, MN, USA

Authors and Affiliations

  1. Department of Civil Engineering, University of Minnesota, 500 Pillsbury Drive SE, Minneapolis, MN, 55455-0116, USA

    Sudeshna Ghosh, Sara J. Ramsden & Timothy M. LaPara

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  1. Sudeshna Ghosh
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  2. Sara J. Ramsden
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  3. Timothy M. LaPara
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Correspondence to Timothy M. LaPara.

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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 84, 791–796 (2009). https://doi.org/10.1007/s00253-009-2125-2

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  • DOI: https://doi.org/10.1007/s00253-009-2125-2

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