Dynamics of antibiotic resistance genes and presence of putative pathogens during ambient temperature anaerobic digestion

Journal of Applied Microbiology

Volumn 117, Issue 6, 2014, Pages 1689-1699

  Resende, J A ^a,b   Diniz, C G ^a   Silva, V L ^a   Otenio, M H ^c   Bonnafous, A ^b   Arcuri, P B ^c   Godon, J J ^b  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^b LABORATOIRE DE BIOTECHNOLOGIE DE L ENVIRONNEMENT   (France)

^c EMBRAPA CERRADOS   (Brazil)

Author keywords

Antibiotics resistance gene abundance; Bacterial pathogens; Biofertilizer dairy cattle manure; Biogas; Seasonal variations

Indexed keywords

ANTIBIOTICS; BACTERIA; BIOGAS; FERTILIZERS; GENES; MANURES; TEMPERATURE;

ANTIBIOTIC RESISTANCE GENE ABUNDANCE; ANTIBIOTIC RESISTANCE GENES; ANTIMICROBIAL RESISTANCES; BACTERIAL PATHOGENS; BIOFERTILIZER DAIRY CATTLE MANURE; BIOFERTILIZERS; DAIRY CATTLE MANURE; PATHOGENIC BACTERIUM; RESISTANCE GENES; SEASONAL VARIATION;

ANAEROBIC DIGESTION;

AMINOGLYCOSIDE ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; MACROLIDE; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; BETA LACTAM; MANURE;

ANOXIC CONDITIONS; ANTIBIOTIC RESISTANCE; DIGESTIBILITY; GENE EXPRESSION; MANURE; PATHOGEN; PERSISTENCE; SEASONAL VARIATION; TEMPERATURE EFFECT;

ACINETOBACTER; ANAEROBIC DIGESTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; APHA2 GENE; ARTICLE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; BLA TEM 1 GENE; CLOSTRIDIUM; DYNAMICS; ENVIRONMENTAL TEMPERATURE; ERMB GENE; GENE; METAGENOMICS; NONHUMAN; SEASONAL VARIATION; STENOTROPHOMONAS; SUMMER; WINTER; ANAEROBIC GROWTH; ANIMAL; BACTERIUM; BIOREACTOR; BOVINE; GENE DOSAGE; GENETICS; ISOLATION AND PURIFICATION; MANURE; MICROBIOLOGY; SEASON; TEMPERATURE;

ACINETOBACTER; BACTERIA (MICROORGANISMS); BOS; CLOSTRIDIUM; STENOTROPHOMONAS;

AMINOGLYCOSIDES; ANAEROBIOSIS; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BETA-LACTAMS; BIOREACTORS; CATTLE; DRUG RESISTANCE, MICROBIAL; GENE DOSAGE; MACROLIDES; MANURE; METAGENOMICS; SEASONS; TEMPERATURE;

EID: 84920932044     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12653     Document Type: Article

References (41)

1. Abubaker, J., Risberg, K. and Pell, M. (2012) Biogas residues as fertilisers - Effects on wheat growth and soil microbial activities. Appl Energy 99, 126-134.
2. Alexander, T.W., Yanke, L.J., Topp, E., Olson, M.E., Read, R.R., Morck, D.W. and McAllister, T.A. (2008) Effect of subtherapeutic administration of antibiotics on the prevalence of antibiotic-resistant Escherichia coli bacteria in feedlot cattle. Appl Environ Microbiol 74, 4405-4416.
3. Alexander, T.W., Yanke, J.L., Reuter, T., Topp, E., Read, R.R., Selinger, B.L. and McAllister, T.A. (2011) Longitudinal characterization of antimicrobial resistance genes in feces shed from cattle fed different subtherapeutic antibiotics. BMC Microbiol 11, 19.
4. American Public Health Association (APHA). (2005) Standard Methods for Examination of Water and Wastewater, 21th edn. Washington, D.C.: American Water Works Association.
5. Beneragama, N., Iwasaki, M., Lateef, S.A., Yamashiro, T., Ihara, I. and Umetsu, K. (2013) The survival of multidrug-resistant bacteria in thermophilic and mesophilic anaerobic co-digestion of dairy manure and waste milk. Anim Sci J 84, 426-433.
6. Burch, T.R., Sadowsky, M.J. and Lapara, T.M. (2013) Aerobic digestion reduces the quantity of antibiotic resistance genes in residual municipal wastewater solids. Front Microbiol 4, 17.
7. Chen, J., Yu, Z., Michel, F.C., Wittum, T. and 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.
8. Diehl, D.L. and LaPara, T.M. (2010) 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 44, 9128-9133.
9. Eikmeyer, F.G., Rademacher, A., Hanreich, A., Hennig, M., Jaenicke, S., Maus, I., Wibberg, D., Zakrzewski, M. et al. (2013) Detailed analysis of metagenome datasets obtained from biogas-producing microbial communities residing in biogas reactors does not indicate the presence of putative pathogenic microorganisms. Biotechnol Biofuels 6, 49.
10. Fonseca, G.P., Cruz, A.G., Faria, J.A.F., Silva, R., Moura, M.R.L. and Carvalho, L.M.J. (2009) Antibiotic residues in Brazilian UHT milk: a screening study. Food Sci Technol 29, 451-453.
11. Ghosh, S. and LaPara, T.M. (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1, 191-203.
12. Heuer, H., Schmitt, H. and Smalla, K. (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14, 236-243.
13. Holm-Nielsen, J.B., Al Seadi, T. and Oleskowicz-Popiel, P. (2009) The future of anaerobic digestion and biogas utilization. Bioresour Technol 100, 5478-5484.
14. Kemper, N. (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8, 1-13.
15. Kunz, A., Steinmetz, R.L.R., Rammeb, M.A. and Coldebella, A. (2009) Effect of storage time on swine manure solid separation efficiency by screening. Bioresour Technol 100, 1815-1818.
16. Lachmayr, K.L., Kerkhof, L.J., Dirienzo, G., Cavanaugh, C.M. and Ford, T.E. (2009) Quantifying nonspecific TEM beta-lactamase (blaTEM) genes in a wastewater stream. Appl Environ Microbiol 75, 203-211.
17. Ma, Y., Wilson, C.A., Novak, J.T., Riffat, R., Aynur, S., Murthy, S. and Pruden, A. (2011) Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environ Sci Technol 45, 7855-7861.
18. Massé, D., Gilbert, Y. and Topp, E. (2011) Pathogen removal in farm-scale psychrophilic anaerobic digesters processing swine manure. Bioresour Technol 102, 641-646.
19. Munir, M. and Xagoraraki, I. (2011) Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J Environ Qual 40, 248.
20. Negreanu, Y., Pasternak, Z., Jurkevitch, E. and Cytryn, E. (2012) Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ Sci Technol 46, 4800-4808.
21. Nero, L.A., Mattos, M.R., Beloti, V., Barros, M.A.F. and Franco, B.D.G.M. (2007) Antimicrobial residues in raw milk from four Brazilian milk-producing regions. Food Sci Technol 27, 391-393.
22. Nõlvak, H., Truu, M., Tiirik, K., Oopkaup, K., Sildvee, T., Kaasik, A., Mander, U. and Truu, J. (2013) Dynamics of antibiotic resistance genes and their relationships with system treatment efficiency in a horizontal subsurface flow constructed wetland. Sci Total Environ 461-462, 636-644.
23. Pribul, B.R., Pereira, I.A., Soares, L.C., Coelho, S.M.O., Barberis, I.L., Pascual, L. and Souza, M.M.S. (2011) Bacterial resistance and bacteriocins action in Staphylococcus aureus isolated from bovine mastitis. Braz J Vet Res An Sci 63, 744-748.
24. Pruden, A., Larsson, D.G.J., Amézquita, A., Collignon, P., Brandt, K.K., Graham, D.W., Lazorchak, J.R., Suzuki, S. et al. (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121, 878-885.
25. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W.G., Peplies, J. and Glockner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA Sequence data compatible with ARB. Nucleic Acids Res 35, 7188-7196.
26. Ramirez, M.S. and Tolmasky, M.E. (2010) Aminoglycoside modifying enzymes. Drug Resist Updat 13, 151-171.
27. Resende, J.A., Silva, V.L., Oliveira, T.L.R., Fortunato, S.O., Carneiro, J.C., Otenio, M.H. and Diniz, C.G. (2014) Prevalence and persistence of potentially pathogenic and antibiotic resistant bacteria during anaerobic digestion treatment of cattle manure. Bioresour Technol 153, 284-291.
28. Roberts, M.C. (2008) Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282, 147-159.
29. Sahlström, L. (2003) A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresour Technol 87, 161-166.
30. Sahlström, L., Aspan, A., Bagge, E., Danielsson-Tham, M.L. and Albihn, A. (2004) Bacterial pathogen incidences in sludge from Swedish sewage treatment plants. Water Res 38, 1989-1994.
31. Salverda, M.L., De Visser, J.A. and Barlow, M. (2010) Natural evolution of TEM-1 b-lactamase: experimental reconstruction and clinical relevance. FEMS Microbiol Rev 34, 1015-1036.
32. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B. et al. (2009) Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75, 7537-7541.
33. Shi, P., Jia, S., Zhang, X.X., Zhang, T., Cheng, S. and Li, A. (2013) Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res 47, 111-120.
34. Snell-Castro, R., Godon, J.J., Delgenès, J.P. and Dabert, P. (2005) Characterization of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis. FEMS Microbiol Ecol 52, 229-242.
35. Syrogiannopoulos, G.A., Grivea, I.N., Ednie, L.M., Bozdogan, B., Katopodis, G.D., Beratis, N.G., Davies, T.A. and Appelbaum, P.C. (2003) Antimicrobial susceptibility and macrolide resistance inducibility of Streptococcus pneumoniae carrying erm(A), erm(B), or mef(A). Antimicrob Agents Chemother 47, 2699-2702.
36. Venglovsky, J., Sasakova, N. and Placha, I. (2009) Pathogens and antibiotic residues in animal manures and hygienic and ecological risks related to subsequent land application. Bioresour Technol 100, 5386-5391.
37. Walsh, J.J., Rousk, J., Edwards-Jones, G., Jones, D.L. and Williams, A.P. (2012) Fungal and bacterial growth following the application of slurry and anaerobic digestate of livestock manure to temperate pasture soils. Biol Fertil Soils 48, 889-897.
38. Wang, Y. and Qian, P. (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PloS one 4, 7401.
39. Wang, L., Oda, Y., Grewal, S., Morrison, M., Michel, F.C. and Yu, Z. (2012) Persistence of resistance to erythromycin and tetracycline in swine manure during simulated composting and lagoon treatments. Microb Ecol 63, 32-40.
40. Watcharasukarn, M., Kaparaju, P., Steyer, J.P., Krogfelt, K. and Angelidaki, I. (2009) Screening Escherichia coli, Enterococcus faecalis, and Clostridium perfringens as indicator organisms in evaluating pathogen-reducing capacity in biogas plants. Microb Ecol 58, 221-230.
41. Yu, Y., Lee, C., Kim, J. and Hwang, S. (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89, 670-679.