Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: Prospects and challenges

Journal of Environmental Quality

Volumn 45, Issue 2, 2016, Pages 441-453

  Luby, Elizabeth ^a   Mark Ibekwe, A ^b   Zilles, Julie ^c   Pruden, Amy ^d  

^a Iowa State University of Science and Technology   (United States)

^b U S SALINITY LABORATORY   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURE; ANTIBIOTICS; GENE TRANSFER; NUCLEIC ACIDS; RESEARCH AND DEVELOPMENT MANAGEMENT;

AGRICULTURAL ECOSYSTEMS; ANTIBIOTIC RESISTANCE; COMPLEMENTARY METHODS; FUTURE APPLICATIONS; HORIZONTAL GENE TRANSFER; MANAGEMENT DECISIONS; MOLECULAR COMPONENTS; POLICY DEVELOPMENT;

ECOSYSTEMS;

ANTIBIOTIC RESISTANCE; ECOSYSTEM; EXPERIMENTAL DESIGN; HUMAN; AGRICULTURE; BACTERIUM; GENETICS;

ANTIINFECTIVE AGENT;

AGRICULTURE; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, MICROBIAL; ECOSYSTEM; HUMANS;

EID: 84960434023     PISSN: 00472425     EISSN: 15372537     Source Type: Journal    
DOI: 10.2134/jeq2015.07.0367     Document Type: Article

References (131)

1. Agerso, Y., and D. Sandvang. 2005. Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. isolated from pigsties and manured soil. Appl. Environ. Microbiol. 71:7941-7947. doi:10.1128/AEM.71.12.7941-7947.2005
2. Agerso, Y., G. Wulff, E. Vaclavik, B. Halling-Sorensen, and L.B. Jensen. 2006. Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet(M) in soil microcosms. Environ. Int. 32:876-882. doi:10.1016/j.envint.2006.05.008
3. Allen, H.K., L.A. Moe, J. Rodbumrer, A. Gaarder, and J. Handelsman. 2009. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME J. 3:243-251. doi:10.1038/ismej.2008.86
4. Allen, H.K., J. Donato, H.H. Wang, K.A. Cloud-Hansen, J. Davies, and J. Handelsman. 2010. Call of the wild: Antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8:251-259. doi:10.1038/nrmicro2312
5. Angenent, L.T., M. Mau, U. George, J.A. Zahn, and L. Raskin. 2008. Effect of the presence of the antimicrobial tylosin in swine waste on anaerobic treatment. Water Res. 42:2377-2384. doi:10.1016/j.watres.2008.01.005
6. Ashbolt, N.J., A. Amezquita, T. Backhaus, P. Borriello, K.K. Brandt, P. Collignon, A. Coors, R. Finley, W.H. Gaze, T. Heberer, J.R. Lawrence, D.G.J. Larrson, S.A. McEwen, J.J. Ryan, J. Schonfeld, P. Silley, J.R. Snape, C. Van den Eede, and E. Topp. 2013. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 121:993-1001.
7. Balcazar, J.L. 2014. Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog. 10:e1004219. doi:10.1371/journal. ppat.1004219
8. Bengtsson-Palme, J., F. Boulund, J. Fick, E. Kristiansson, and D.G.J. Larsson. 2014. Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front. Microbiol. 5:1-14.
9. Berendonk, T.U., C.M. Manaia, C. Merlin, D. Fatta-Kassinos, E. Cytryn, F. Walsh, H. Buergmann, H. Sorum, M. Norstrom, M.N. Pons, et al. 2015. Tackling antibiotic resistance: The environmental framework. Nat. Rev. Microbiol. 13:310-317. doi:10.1038/nrmicro3439
10. Binh, C.T.T., H. Heuer, M. Kaupenjohann, and K. Smalla. 2008. Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol. Ecol. 66:25-37. doi:10.1111/j.1574-6941.2008.00526.x
11. Brabban, A.D., E. Hite, and T.R. Callaway. 2005. Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer. Foodborne Pathog. Dis. 2:287-303. doi:10.1089/fpd.2005.2.287
12. Canchaya, C., C. Proux, G. Fournous, A. Bruttin, and H. Brussow. 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:238-276. doi:10.1128/MMBR.67.2.238-276.2003
13. Carattoli, A., A. Bertini, L. Villa, V. Falbo, K.L. Hopkins, and E.J. Threlfall. 2005. Identification of plasmids by PCR-based replicon typing. J. Microbiol. Methods 63:219-228. doi:10.1016/j.mimet.2005.03.018
14. Casjens, S. 2003. Prophages and bacterial genomics: What have we learned so far? Mol. Microbiol. 49:277-300. doi:10.1046/j.1365-2958.2003.03580.x
15. Chee-Sanford, J.C., R.I. Aminov, I.J. Krapac, N. Garrigues-Jeanjean, and R.I. Mackie. 2001. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67:1494-1502. doi:10.1128/AEM.67.4.1494-1502.2001
16. Chen, I., and D. Dubnau. 2004. DNA uptake during bacterial transformation. Nat. Rev. Microbiol. 2:241-249. doi:10.1038/nrmicro844
17. Cochetti, I., E. Tili, M. Vecchi, A. Manzin, M. Mingoia, P.E. Varaldo, and M.P. Montanari. 2007. New Tn916-related elements causing erm(B)-mediated erythromycin resistance in tetracycline-susceptible pneumococci. J. Antimicrob. Chemother. 60:127-131. doi:10.1093/jac/dkm120
18. Cochetti, I., E. Tili, M. Mingoia, P.E. Varaldo, and M.P. Montanari. 2008. Erm(B)-carrying elements in tetracycline-resistant pneumococci and correspondence between Tn1545 and Tn6003. Antimicrob. Agents Chemother. 52:1285-1290. doi:10.1128/AAC.01457-07
19. Colomer-Lluch, M., L. Imamovic, J. Jofre, and M. Muniesa. 2011a. Bacteriophages carrying antibiotic resistance genes in fecal waste from cattle, pigs, and poultry. Antimicrob. Agents Chemother. 55:4908-4911. doi:10.1128/AAC.00535-11
20. Colomer-Lluch, M., J. Jofre, and M. Muniesa. 2011b. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6:e17549. doi:10.1371/journal.pone.0017549
21. Coque, T.M., F. Baquero, and R. Cantón. 2008. Increasing prevalence of ESBLproducin Enterobacteriaceae in Europe. Euro Surveill. 13:5437-5453.
22. Couturier, M., F. Bex, P.L. Berquist, and W.K. Maas. 1988. Identification and classification of bacterial plasmids. Microbiol. Rev. 52:375-395.
23. de Castro, A.P., G.D.R. Fernandes, and O.L. Franco. 2014. Insights into novel antimicrobial compounds and antibiotic resistance genes from soil metagenomes. Front. Microbiol. 5:1-9.
24. Del Grosso, M., R. Camilli, B. Libisch, M. Fuzi, and A. Pantosti. 2009. New composite genetic element of the Tn916 family with dual macrolide resistance genes in a Streptococcus pneumonia isolate belonging to clonal complex 271. Antimicrob. Agents Chemother. 53:1293-1294. doi:10.1128/AAC.01066-08
25. Demaneche, S., E. Kay, F. Gourbiere, and P. Simonet. 2001. Natural transformation of Pseudomonas fluorescens and Agrobacterium tumefaciens in soil. Appl. Environ. Microbiol. 67:2617-2621. doi:10.1128/AEM.67.6.2617-2621.2001
26. Dodd, M.C. 2012. Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J. Environ. Monit. 14:1754-1771. doi:10.1039/c2em00006g
27. Donato, J.J., L.A. Moe, B.J. Converse, K.D. Smart, F.C. Berklein, P.S. McManus, and J. Handelsman. 2010. Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl. Environ. Microbiol. 76:4396-4401. doi:10.1128/AEM.01763-09
28. Durso, L.M., D.N. Miller, and B. Wienhold. 2012. Distribution and quantification of antibiotic resistant genes and bacteria across agricultural and nonagricultural metagenomes. PLoS One 7:e48325. doi:10.1371/journal. pone.0048325
29. Engemann, C.A., P.L. Keen, C.W. Knapp, K.J. Hall, and D.W. Graham. 2008. Fate of tetracycline resistance genes in aquatic systems: Migration from the water column to peripheral biofilms. Environ. Sci. Technol. 42:5131-5136. doi:10.1021/es800238e
30. Facinelli, B., M.C. Roberts, E. Giofanetti, C. Casolari, U. Fabio, and P.E. Varaldo. 1993. Genetic-basis of tetracycline resistance in food-borne isolates of Listeria innocua. Appl. Environ. Microbiol. 59:614-616.
31. Fang, H., H.F. Wang, L. Cai, and Y.L. Yu. 2015. Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environ. Sci. Technol. 49:1095-1104. doi:10.1021/es504157v
32. Fineran, P.C., N.K. Petty, and G.P.C. Salmond. 2009. Transduction: Host DNA transfer by bacteriophages. In: M. Schaechter, editor, The desk encyclopedia of microbiology. Elsevier Academic Press, San Diego, CA. p. 666-679.
33. Forsberg, K.J., S. Patel, M.K. Gibson, C.L. Lauber, R. Knight, N. Fierer, and G. Dantas. 2014. Bacterial phylogeny structures soil resistomes across habitats. Nature 509:612-615. doi:10.1038/nature13377
34. Forsberg, K.J., A. Reyes, B. Wang, E.M. Selleck, and M.O. Sommer. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111. doi:10.1126/science.1220761
35. Frost, L.S., R. Leplae, A.O. Summers, and A. Toussaint. 2005. Mobile genetic elements: The agents of open source evolution. Nat. Rev. Microbiol. 3:722-732. doi:10.1038/nrmicro1235
36. Garder, J.L., T.B. Moorman, and M.L. Soupir. 2014. Transport and persistence of tylosin-resistant enterococci, erm genes, and tylosin in soil and drainage water from fields receiving swine manure. J. Environ. Qual. 43:1484-1493. doi:10.2134/jeq2013.09.0379
37. Gibson, M.K., K.J. Forsberg, and G. Dantas. 2015. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9:207-216. doi:10.1038/ismej.2014.106
38. Gillespie, D.E., S.F. Brady, A.D. Bettermann, N.P. Cianciotto, M.R. Liles, and M.R. Rondon. 2002. Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl. Environ. Microbiol. 68:4301-4306. doi:10.1128/AEM.68.9.4301-4306.2002
39. Goessweiner-Mohr, N., K. Arends, W. Keller, and E. Grohmannc. 2013. Conjugative type IV secretion systems in Gram-positive bacteria. Plasmid 70:289-302. doi:10.1016/j.plasmid.2013.09.005
40. Gotz, A., R. Pukail, E. Smit, E. Tietze, R. Prager, H. Tschape, J.D. Van Elsas, and K. Smalla. 1996. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl. Environ. Microbiol. 62:2621-2628.
41. Goyer, C., and C.E. Dandie. 2012. Quantification of microorganisms targeting conserved genes in complex environmental samples using quantitative polymerase chain reaction. In: M. Filion, editor, Quantitative real-time PCR in applied microbiology. Horizon Press, Portland, OR. p. 87-106.
42. Guo, F., and T. Zhang. 2013. Biases during DNA extraction of activated sludge samples revealed by high throughput sequences. Appl. Microbiol. Biotechnol. 97:4607-4616.
43. Henry, C.S., R. Overbeek, F.F. Xia, A.A. Best, E. Glass, J. Gilbert, P. Larsen, R. Edwards, T. Disz, F. Meyer, et al. 2011. Connecting genotype to phenotype in the era of high-throughput sequencing. Biochim. Biophys. Acta. 1810(10):967-977.
44. Heuer, H., and K. Smalla. 2007. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ. Microbiol. 9:657-666. doi:10.1111/j.1462-2920.2006.01185.x
45. Heuer, H., H. Schmitt, and K. Smalla. 2011a. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14:236-243. doi:10.1016/j.mib.2011.04.009
46. Heuer, H., Q. Solehati, U. Zimmerling, K. Kleineidam, M. Schloter, T. Muller, A. Focks, S. Thiele-Bruhn, and K. Smalla. 2011b. Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl. Environ. Microbiol. 77:2527-2530. doi:10.1128/AEM.02577-10
47. Hoorfar, J., B. Malorney, A. Abdulmawjood, N. Cook, M. Wagner, and P. Fach. 2004. Practical considerations in design of internal amplification controls for diagnostic PCR assays. J. Clin. Microbiol. 42:1863-1868. doi:10.1128/JCM.42.5.1863-1868.2004
48. Jindal, A., S. Kocherginskaya, A. Mehboob, M. Robert, R.I. Mackie, L. Raskin, and J.L. Zilles. 2006. Antimicrobial use and resistance in swine waste treatment systems. Appl. Environ. Microbiol. 72:7813-7820. doi:10.1128/AEM.01087-06
49. Johnston, C., B. Martin, G. Fichant, P. Polard, and J.P. Claverys. 2014. Bacterial transformation: Distribution, shared mechanisms and divergent control. Nat. Rev. Microbiol. 12:181-196. doi:10.1038/nrmicro3199
50. Klümper, U., I. Riber, A. Dechesne, A. Sannazzarro, L.H. Hansen, S.J. Sorensen, and B.F. Smets. 2015. Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community. ISME J. 9:934-945. doi:10.1038/ismej.2014.191
51. Knapp, C.W., J. Dolfing, P.A.I. Ehlert, and D.W. Graham. 2010. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44:580-587. doi:10.1021/es901221x
52. Koike, S., I.G. Krapac, H.D. Oliver, A.C. Yannarell, J.C. Chee-Sanford, R.I. Aminov, and R.I. Mackie. 2007. Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Appl. Environ. Microbiol. 73:4813-4823. doi:10.1128/AEM.00665-07
53. Kristiansson, E., J. Fick, A. Janzon, R. Grabic, C. Rutgersson, B. Weijdegard, H. Soderstrom, and D.G.J. Larsson. 2011. Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6:e17038. doi:10.1371/journal.pone.0017038
54. Lang, K.S., J.M. Anderson, S. Schwarz, L. Williamson, J. Handelsman, and R.S. Singer. 2010. Novel florfenicol and chloramphenicol resistance gene discovered in Alaskan soil by using functional metagenomics. Appl. Environ. Microbiol. 76:5321-5326. doi:10.1128/AEM.00323-10
55. Lennon, J.T. 2011. Replication, lies and lesser-known truths regarding experimental design in environmental microbiology. Environ. Microbiol. 13:1383-1386. doi:10.1111/j.1462-2920.2011.02445.x
56. Levy-Booth, D.J., R.G. Campbell, R.H. Gulden, M.M. Hart, J.R. Powell, J.N. Klironomos, K.P. Pauls, C.J. Swanton, J.T. Trevors, and K.E. Dunfield. 2007. Cycling of extracellular DNA in the soil environment. Soil Biol. Biochem. 39:2977-2991. doi:10.1016/j.soilbio.2007.06.020
57. Li, L., N. Mendis, H. Triqui, J.D. Oliver, and S.P. Faucher. 2014. The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol. 5:1-20.
58. Liao, Y.T., S.C. Kuo, Y.T. Lee, C.P. Chen, S.W. Lin, L.J. Shen, C.P. Fung, W.L. Cho, and T.L. Chen. 2014. Sheltering effect and indirect pathogenesis of carbapenem-resistant Acinetobacter baumannii in polymicrobial infection. Antimicrob. Agents Chemother. 58:3983-3990. doi:10.1128/AAC.02636-13
59. Lim, H.K., E.J. Chung, J.C. Kim, G.J. Choi, K.S. Jang, and Y.R. Chung. 2005. Characterization of a forest soil metagenome clone that confers indirubin and indigo production on Escherichia coli. Appl. Environ. Microbiol. 71:7768-7777. doi:10.1128/AEM.71.12.7768-7777.2005
60. Looft, T., T.A. Johnson, H.K. Allen, D.O. Bayles, D.P. Alt, R.D. Stedtfeld, W.J. Sul, T.M. Stedtfeld, B. Chai, J.R. Cole, S.A. Hashsham, J.M. Tiedje, and T.B. Stanton. 2012. In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl. Acad. Sci. USA 109:1691-1696. doi:10.1073/pnas.1120238109
61. Lorenz, M.G., and W. Wackernagel. 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58:563-602.
62. Lu, N., J.L. Zilles, and T.H. Nguyen. 2010. Adsorption of extracellular chromosomal DNA and its effects on natural transformation of Azotobacter vinelandii. Appl. Environ. Microbiol. 76:4179-4184. doi:10.1128/AEM.00193-10
63. Luo, G., and I. Angelidaki. 2014. Analysis of bacterial communities and bacterial pathogens in a biogas plant by the combination of ethidium monoazide, PCR and Ion Torrent sequencing. Water Res. 60:156-163. doi:10.1016/j. watres.2014.04.047
64. MacNeil, I.A., C.L. Tiong, C. Minor, P.R. Augus, T.H. Grossman, and K.A. Loiacono. 2001. Expression and isolation of antimicrobial small molecules from soil DNA libraries. J. Mol. Microbiol. Biotechnol. 3:301-308.
65. Maier, T., M. Güell, and L. Serrano. 2009. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583:3966-3973. doi:10.1016/j. febslet.2009.10.036
66. Malik, A., E.K. Celik, C. Bohn, U. Bockelmann, K. Knobel, and E. Grohmann. 2008. Detection of conjugative plasmids and antibiotic resistance genes in anthropogenic soils from Germany and India. FEMS Microbiol. Lett. 279:207-216. doi:10.1111/j.1574-6968.2007.01030.x
67. Markowitz, V.M., I.M.A. Chen, K. Palaniappan, K. Chu, and E. Szeto. 2012. IMG: The integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 40:D115-D122. doi:10.1093/nar/gkr1044
68. Marti, R., A. Scott, Y.C. Tien, R. Murray, L. Sabourin, Y. Zhang, and E. Topp. 2013. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl. Environ. Microbiol. 79:5701-5709. doi:10.1128/AEM.01682-13
69. McArthur, A.G., N. Waglechner, F. Nizam, A. Yan, M.A. Azad, A.J. Baylay, K. Bhullar, M.J. Canova, G. De Pascale, L. Ejim, L. Kalan, A.M. King, K. Koteva, M. Morar, M.R. Mulvey, J.S. O'Brien, A.C. Pawlowski, L.J. Piddock, P. Spanogiannopoulos, A.D. Sutherland, I. Tang, P.L. Taylor, M. Thaker, W. Wang, M. Yan, T. Yu, and G.D. Wright. 2013. The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 57:3348-3357. doi:10.1128/AAC.00419-13
70. McGarvey, K.M., K. Queitsch, and S. Fields. 2012. Wide variation in antibiotic resistance proteins identified by functional metagenomic screening of a soil DNA library. Appl. Environ. Microbiol. 78:1708-1714. doi:10.1128/AEM.06759-11
71. McKinney, C.W., K.A. Loftin, M.T. Meyer, J.G. Davis, and A. Pruden. 2010. Tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environ. Sci. Technol. 44:6102-6109. doi:10.1021/es9038165
72. McKinney, C.W., and A. Pruden. 2012. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 46(24):13393-13400. doi:1 0.1021/es303652q
73. Meyer, F., D. Paarmann, M. D'Souza, R. Olson, E.M. Glass, M. Kubal, T. Paczian, A. Rodriguez, R. Stevens, A. Wilke, J. Wilkening, and R.A. Edwards. 2008. The metagenomics RAST server: A public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf. 9:386. doi:10.1186/1471-2105-9-386
74. Mezger, A., E. Gullberg, J. Göransson, A. Zorzet, D. Herthnek, E. Tano, M. Nilsson, and D.I. Andersson. 2015. A general method to rapidly determine antibiotic susceptibility and species in bacterial infections. J. Clin. Microbiol. 53:425-432. doi:10.1128/JCM.02434-14
75. Musovic, S., A. Dechesne, J. Sorensen, and B.F. Smets. 2010. Novel assay to assess permissiveness of a soil microbial community toward receipt of mobile genetic elements. Appl. Environ. Microbiol. 76:4813-4818. doi:10.1128/AEM.02713-09
76. Musovic, S., U. Klümper, A. Dechesne, J. Magid, and B.F. Smets. 2014. Long-term manure exposure increases soil bacterial community potential for plasmid uptake. Environ. Microbiol. Rep. 6:125-130. doi:10.1111/1758-2229.12138
77. Nandi, S., J.J. Maurer, C. Hofacre, and A.O. Summers. 2004. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101:7118-7122. doi:10.1073/pnas.0306466101
78. Nesme, J., S. Cécillon, T.O. Delmont, J.M. Monier, T.M. Vogel, and P. Simonet. 2014. Large-scale metagenomic-based study of antibiotic resistance in the environment. Curr. Biol. 24:1096-1100. doi:10.1016/j.cub.2014.03.036
79. Nesme, J., and P. Simonet. 2015. The soil resistome: A critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ. Microbiol. 17:913-930. doi:10.1111/1462-2920.12631
80. Nielsen, K.M., M.D.M. Van Weerelt, T.N. Berg, A.M. Bones, A.N. Hagler, and J.D. Van Elsas. 1997. Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms. Appl. Environ. Microbiol. 63:1945-1952.
81. Nocker, A., C.Y. Cheung, and A.K. Camper. 2006. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Methods 67:310-320. doi:10.1016/j.mimet.2006.04.015
82. Ochman, H., J.G. Lawrence, and E.A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304. doi:10.1038/35012500
83. Peak, N., C.W. Knapp, R.K. Yang, M.M. Hanfelt, M.S. Smith, D.S. Aga, and D.W. Graham. 2007. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol. 9:143-151. doi:10.1111/j.1462-2920.2006.01123.x
84. Pehrsson, E.C., K.J. Forsberg, M.K. Gibson, S. Ahmadi, and G. Dantas. 2013. Novel resistance functions uncovered using functional metagenomic investigations of resistance reservoirs. Front. Microbiol. 4:145.
85. Pei, R., S.C. Kim, K.H. Carlson, and A. Pruden. 2006. Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res. 40:2427-2435. doi:10.1016/j. watres.2006.04.017
86. Pei, R., J.M. Cha, K.H. Carlson, and A. Pruden. 2007. Biological treatment of antibiotic resistance genes (ARG) in dairy lagoon water. Environ. Sci. Technol. 41(14):50018-5013. doi:10.1016/j.watres.2006.04.017
87. Perry, J.A., and G.D. Wright. 2013. The antibiotic resistance "mobilone": Searching for the link between environment and clinic. Front. Microbiol. 4:138. doi: 10.3389/fmicb.2013.00138
88. Pietramellara, G., J. Ascher, F. Borgogni, M.T. Ceccherini, G. Guerri, and P. Nannipieri. 2009. Extracellular DNA in soil and sediment: Fate and ecological relevance. Biol. Fertil. Soils 45:219-235. doi:10.1007/s00374-008-0345-8
89. Popowska, M., M. Rzeczycka, A. Miernik, A. Krawczyk-Balska, F. Walsh, and B. Duffy. 2011. Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob. Agents Chemother. 350:180-189.
90. Port, J.A., J.C. Wallace, W.C. Griffith, and E.M. Faustman. 2012. Metagenomic profiling of microbial composition and antibiotic resistance determinants in Puget Sound. PLoS One 7:E48000. doi:10.1371/journal.pone.0048000
91. Prosser, J.I. 2010. Replicate or lie. Environ. Microbiol. 12:1806-1810. doi:10.1111/j.1462-2920.2010.02201.x
92. Pruden, A., R. Pei, H. Storteboom, and K.H. Carlson. 2006. Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environ. Sci. Technol. 40:7445-7450. doi:10.1021/es060413l
93. Pruden, A., M. Arabi, and H.N. Storteboom. 2012. Correlation between upstream human activities and riverine antibiotic resistance genes. Environ. Sci. Technol. 46:11541-11549. doi:10.1021/es302657r
94. Ray, J.L., and K.M. Nielsen. 2005. Experimental methods for assaying natural transformation and inferring horizontal gene transfer. Methods Enzymol. 395:491-520. doi:10.1016/S0076-6879(05)95026-X
95. Renaud, C.S., J.J. Pasternak, and B.R. Glick. 1989. Integration of exogenous DNA into the genome of Azotobacter vinelandii. Arch. Microbiol. 152:437-440. doi:10.1007/BF00446925
96. Roberts, A.P., I.J. Davis, L. Seville, A. Villedieu, and P. Mullany. 2006. Characterization of the ends and target site of a novel tetracycline resistance encoding conjugative transposon from Enterococcus faecium 664.1H1. J. Bacteriol. 188:4356-4361. doi:10.1128/JB.00129-06
97. Roberts, A.P., and P. Mullany. 2011. Tn916-like genetic elements: A diverse group of modular mobile elements conferring antibiotic resistance. FEMS Microbiol. Rev. 35:856-871. doi:10.1111/j.1574-6976.2011.00283.x
98. Roberts, M.C. 2012. Acquired tetracycline resistance genes. In: T.J. Dougherty and M.J. Pucci, editors, Antibiotic discovery and development. Vol. 1 and 2. Springer, New York. p. 543-568.
99. Rodríguez, R.A., S. Bounty, and K.G. Linden. 2013. Long-range quantitative PCR for determining inactivation of adenovirus 2 by ultraviolet light. J. Appl. Microbiol. 114:1854-1865. doi:10.1111/jam.12169
100. Rothrock, M.J., Jr., P.L. Keen, K.L. Cook, L.M. Durso, A.M. Franklin, and R.S. Dungan. 2016. How should we be determining background and baseline antibiotic resistance levels in agroecosystem research? J. Environ. Qual. doi:10.2134/jeq2015.06.0327 (in press).
101. Rudi, K., B. Moen, S.M. Dromtorp, and A.L. Holck. 2005. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl. Environ. Microbiol. 71:1018-1024. doi:10.1128/AEM.71.2.1018-1024.2005
102. Sato, T., T. Okubo, M. Usui, S. Yokota, S. Izumiyama, and Y. Tamura. 2014. Association of veterinary third-generation cephalosporin use with the risk of emergence of extended-spectrum-cephalosporin resistance in Escherichia coli from dairy cattle in Japan. PLoS One 9:e96101. doi:10.1371/journal. pone.0096101
103. Schlüter, A., R. Szczepanowski, A. Pühler, and E.M. Top. 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. doi:10.1111/j.1574-6976.2007.00074.x
104. Schmieder, R., and R. Edwards. 2012. Insights into antibiotic resistance through metagenomics approaches. Future Microbiol. 7:73-89. doi:10.2217/fmb.11.135
105. Schmieger, H., and P. Schicklmaier. 1999. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol. Lett. 170:251-256. doi:10.1111/j.1574-6968.1999.tb13381.x
106. Seitz, P., and M. Blokesch. 2013. Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental Gram-negative bacteria. FEMS Microbiol. Rev. 37:336-363. doi:10.1111/j.1574-6976.2012.00353.x
107. Smalla, K., and P.A. Sobecky. 2002. The prevalence and diversity of mobile genetic elements in bacterial communities of different environmental habitats: Insights gained from different methodological approaches. FEMS Microbiol. Ecol. 42:165-175. doi:10.1111/j.1574-6941.2002.tb01006.x
108. Smith, M.S., R.K. Yang, C.W. Knapp, Y. Niu, N. Peak, M.M. Hanfelt, J.C. Galland, and D.W. Graham. 2004. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl. Environ. Microbiol. 70:7372-7377. doi:10.1128/AEM.70.12.7372-7377.2004
109. Stewart, P.S., and J.W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. J. Lancet 358:135-138. doi:10.1016/S0140-6736(01)05321-1
110. Storteboom, H., M. Arabi, J.G. Davis, B. Crimi, and A. Pruden. 2010. Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environ. Sci. Technol. 44:1947-1953. doi:10.1021/es902893f
111. Su, J.Q., B. Wei, C.Y. Xu, M. Qiao, and Y.G. Zhu. 2014. Functional metagenomic characterization of antibiotic resistance genes in agricultural soils from China. Environ. Int. 65:9-15. doi:10.1016/j.envint.2013.12.010
112. Suess, J., S. Volz, U. Obst, and T. Schwartz. 2009. Application of a molecular biology concept for the detection of DNA damage and repair during UV disinfection. Water Res. 43:3705-3716. doi:10.1016/j.watres.2009.05.048
113. Thames, C.H., A. Pruden, R.E. James, P.P. Ray, and K.F. Knowlton. 2012. Excretion of antibiotic resistance genes by dairy calves fed milk replacers with varying doses of antibiotics. Front. Microbiol. 10:139.
114. The White House. 2015. National action plan for combatting antibiotic resistant bacteria. www.whitehouse.gov/sites/default/files/docs/national_action_plan_for_combating_antibotic-resistant_bacteria.pdf (accessed 9 Dec. 2015).
115. Thomas, T., J. Gilbert, and M. Folker. 2012. Metagenomics: A guide from sampling to data analysis. Microb. Inform. Exp. 2:3. doi:10.1186/2042-5783-2-3
116. Trebesius, K.H., K. Panthel, S. Strobel, K. Vogt, G. Faller, T. Kirchner, M. Kist, J. Heesemann, and R. Haas. 2000. Rapid and specific detection of Helicobacter pylori macrolide resistance in gastric tissue by fluorescent in situ hybridisation. Gut 46:608-614. doi:10.1136/gut.46.5.608
117. Tsubakishita, S., K. Kuwahara-Arai, T. Sasaki, and K. Hiramatsu. 2010. Origin and molecular evolution of the determinant of methicillin resistance in staphylococci. Antimicrob. Agents Chemother. 54:4352-4359. doi:10.1128/AAC.00356-10
118. Uchiyama, T., and K. Miyazaki. 2009. Functional metagenomics for enzyme discovery: Challenges to efficient screening. Curr. Opin. Biotechnol. 20:616-622. doi:10.1016/j.copbio.2009.09.010
119. Udikovic-Kolic, N., F. Wichmann, N.A. Broderick, and J. Handelsman. 2014. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc. Natl. Acad. Sci. USA 111:15202-15207. doi:10.1073/pnas.1409836111
120. Wagner, M., H. Smidt, A. Loy, and J. Zhou. 2007. Unravelling microbial communities with DNA-microarrays: Challenges and future directions. Microb. Ecol. 53:498-506. doi:10.1007/s00248-006-9197-7
121. Wang, F.H., M. Qiao, J.Q. Su, Z. Chen, X. Zhou, and Y.G. Zhu. 2014. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ. Sci. Technol. 48:9079-9085. doi:10.1021/es502615e
122. Wichmann, F., N. Udikovic-Kolic, S. Andrew, and J. Handelsman. 2014. Diverse antibiotic resistance genes in dairy cow manure. MBio 5:e01017-e13.
123. Wilson, I.G. 1997. Inhibition and facilitation of nucleic acid amplification. Appl. Environ. Microbiol. 63:3741-3751.
124. Witte, W. 2004. International dissemination of antibiotic resistant strains of bacterial pathogens. Infect. Genet. Evol. 4:187-191. doi:10.1016/j. meegid.2003.12.005
125. Yang, Y., X.T. Jiang, and T. Zhang. 2014. Evaluation of a hybrid approach using UBLAST and BLASTX for metagenomic sequences annotation of specific functional genes. PLoS One 9:e110947. doi:10.1371/journal. pone.0110947
126. Zechner, E.L., F. de la Cruz, R. Eisenbrandt, A.M. Grahn, G. Koraimann, E. Lanka, G. Muth, W. Pansegrau, C.M. Thomas, B.M. Wilkens, and M. Ztayka. 2003. Conjugative-DNA transfer processes. In: C.M. Thomas, editor, Horizontal gene pool: Bacterial plasmids and gene spread. CRC Press, Boca Raton, FL. p. 93-174.
127. Zhang, Y., D.D. Snow, D. Parker, Z. Zhou, and X. Li. 2013. Intracellular and extracellular antimicrobial resistance genes in the sludge of livestock waste management structures. Environ. Sci. Technol. 47:10206-10213.
128. Zhou, Z., L. Raskin, and J.L. Zilles. 2009. Identification of macrolide resistant microorganisms on antimicrobial-free swine farms. Appl. Environ. Microbiol. 75:5814-5820. doi:10.1128/AEM.00977-09
129. Zhou, W., L. Raskin, and J.L. Zilles. 2010. Effects of swine manure on macrolide, licosamide, and streptogramin B antimicrobial resistance in soils. Appl. Environ. Microbiol. 78:3028-3032. doi:10.1128/AEM.06920-11
130. Zhou, W., Y. Wang, and J. Lin. 2012. Functional cloning and characterization of antibiotic resistance genes from the chicken gut microbiome. Appl. Environ. Microbiol. 78:3028-3032. doi:10.1128/AEM.06920-11
131. Zhu, Y.G., T.A. Johnson, T.Q. Su, M. Qiao, G.X. Guo, R.D. Stedtfeld, S.A. Hashsham, and J.M. Tiedje. 2013. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. USA 110:3435-3440. doi:10.1073/pnas.1222743110