Potential Dissemination of ARB and ARGs into Soil Through the Use of Treated Wastewater for Agricultural Irrigation: Is It a True Cause for Concern?

  • Nada Al-Jassim
  • Pei-Ying HongEmail author
Part of the Soil Biology book series (SOILBIOL, volume 51)


Resistance to antibiotics is increasingly being recognized as an emerging contaminant posing great risks to effective treatment of infections and to public health. Pristine soils or even soils that predate the antibiotic era naturally contain ARB and ARGs. This book chapter explores the native resistome of soils and collates information on whether soil perturbation through wastewater reuse can lead to accumulation of ARB and ARGs in agricultural soils. Special emphasis was given to ARGs, particularly the bla NDM gene that confers resistance against carbapenem. The fate and persistence of these emerging ARGs have not been studied in depth; however, this book chapter reviews available information on other ARGs to gain insight into the possibility of horizontal gene transfer events in wastewater-irrigated soils and plant surfaces and tissues. Lastly, this book chapter visits solar irradiation and bacteriophage treatment as intervention options to limit dissemination of emerging contaminant threats.


Antibiotic resistance New Delhi metallo-beta-lactamase Horizontal gene transfer Solar inactivation Bacteriophage 


  1. Al-Jasser AO (2011) Saudi wastewater reuse standards for agricultural irrigation: Riyadh treatment plants effluent compliance. J King Saud Univ Eng Sci 23(1):1–8CrossRefGoogle Scholar
  2. Al-Jassim N, Ansari MI, Harb M, Hong P-Y (2015) Removal of bacterial contaminants and antibiotic resistance genes by conventional wastewater treatment processes in Saudi Arabia: is the treated wastewater safe to reuse for agricultural irrigation? Water Res 73:277–290PubMedCrossRefGoogle Scholar
  3. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J (2009) Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil. ISME J 3(2):243–251PubMedCrossRefGoogle Scholar
  4. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8(4):251–259PubMedCrossRefGoogle Scholar
  5. Araki M (1986) Advanced slime control process with bacteriophage. Kogyo Yosui 332:25–30Google Scholar
  6. Arpin C, Noury P, Boraud D, Coulange L, Manetti A, Andre C, M’Zali F, Quentin C (2012) NDM-1-producing Klebsiella pneumoniae resistant to colistin in a French community patient without history of foreign travel. Antimicrob Agents Chemother 56(6):3432–3434PubMedPubMedCentralCrossRefGoogle Scholar
  7. Balogh B, Jones JB, Iriarte F, Momol M (2010) Phage therapy for plant disease control. Curr Pharm Biotechnol 11(1):48–57PubMedCrossRefGoogle Scholar
  8. Barak JD, Liang AS (2008) Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS One 3(2):e1657PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bell K, Sebaihia M, Pritchard L, Holden M, Hyman L, Holeva M, Thomson N, Bentley S, Churcher L, Mungall K (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101(30):11105–11110PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks ED, Johnston MD, Barton HA, Wright GD (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7(4):e34953PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bichai F, Polo-López MI, Ibañez PF (2012) Solar disinfection of wastewater to reduce contamination of lettuce crops by Escherichia coli in reclaimed water irrigation. Water Res 46(18):6040–6050PubMedCrossRefGoogle Scholar
  12. Blough NV, Zepp RG (1995) Reactive oxygen species in natural waters. In: Foote CS, Valentine JS, Greenberg A, Liebman JF (eds) Active oxygen in chemistry. Springer, Dordrecht, pp 280–333CrossRefGoogle Scholar
  13. Boehm AB, Yamahara KM, Love DC, Peterson BM, McNeill K, Nelson KL (2009) Covariation and photoinactivation of traditional and novel indicator organisms and human viruses at a sewage-impacted marine beach. Environ Sci Technol 43(21):8046–8052PubMedCrossRefGoogle Scholar
  14. Bolton NF, Cromar NJ, Hallsworth P, Fallowfield HJ (2010) A review of the factors affecting sunlight inactivation of micro-organisms in waste stabilisation ponds: preliminary results for enterococci. Water Sci Technol 61(4):885–890PubMedCrossRefGoogle Scholar
  15. Bonnin RA, Poirel L, Carattoli A, Nordmann P (2012) Characterization of an IncFII plasmid encoding NDM-1 from Escherichia coli ST131. PLoS One 7(4):e34752PubMedPubMedCentralCrossRefGoogle Scholar
  16. Borgia S, Lastovetska O, Richardson D, Eshaghi A, Xiong J, Chung C, Baqi M, McGeer A, Ricci G, Sawicki R, Pantelidis R, Low DE, Patel SN, Melano RG (2012) Outbreak of carbapenem-resistant enterobacteriaceae containing blaNDM-1, Ontario, Canada. Clin Infect Dis 55(11):e109–e117PubMedCrossRefGoogle Scholar
  17. Boyle M, Sichel C, Fernandez-Ibanez P, Arias-Quiroz GB, Iriarte-Puna M, Mercado A, Ubomba-Jaswa E, McGuigan KG (2008) Bactericidal effect of solar water disinfection under real sunlight conditions. Appl Environ Microbiol 74(10):2997–3001PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brandl M (2008) Plant lesions promote the rapid multiplication of Escherichia coli O157: H7 on postharvest lettuce. Appl Environ Microbiol 74(17):5285–5289PubMedPubMedCentralCrossRefGoogle Scholar
  19. Brockhurst M, Buckling A, Rainey P (2006) Spatial heterogeneity and the stability of host-parasite coexistence. J Evol Biol 19(2):374–379PubMedCrossRefGoogle Scholar
  20. Brown MG, Balkwill DL (2009) Antibiotic resistance in bacteria isolated from the deep terrestrial subsurface. Microb Ecol 57(3):484PubMedCrossRefGoogle Scholar
  21. Bush K (2010) Alarming β-lactamase-mediated resistance in multidrug-resistant Enterobacteriaceae. Curr Opin Microbiol 13(5):558–564PubMedCrossRefGoogle Scholar
  22. Canonica S, Kohn T, Mac M, Real FJ, Wirz J, von Gunten U (2005) Photosensitizer method to determine rate constants for the reaction of carbonate radical with organic compounds. Environ Sci Technol 39(23):9182–9188PubMedCrossRefGoogle Scholar
  23. Carattoli A, Villa L, Poirel L, Bonnin RA, Nordmann P (2012) Evolution of IncA/C blaCMY-2-carrying plasmids by acquisition of the blaNDM-1 carbapenemase gene. Antimicrob Agents Chemother 56(2):783–786PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chen H, Zhang M (2013) Effects of advanced treatment systems on the removal of antibiotic resistance genes in wastewater treatment plants from Hangzhou, China. Environ Sci Technol 47(15):8157–8163PubMedGoogle Scholar
  25. Choi J, Kotay SM, Goel R (2011) Bacteriophage-based biocontrol of biological sludge bulking in wastewater. Bioengineered Bugs 2(4):214–217PubMedCrossRefGoogle Scholar
  26. Corin N, Backlund P, Kulovaara M (1996) Degradation products formed during UV-irradiation of humic waters. Chemosphere 33(2):245–255CrossRefGoogle Scholar
  27. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158(1):41–64PubMedPubMedCentralGoogle Scholar
  28. Curtis TP, Mara DD, Silva SA (1992) Influence of pH, oxygen, and humic substances on ability of sunlight to damage fecal coliforms in waste stabilization pond water. Appl Environ Microbiol 58(4):1335–1343PubMedPubMedCentralGoogle Scholar
  29. Cytryn E (2013) The soil resistome: the anthropogenic, the native, and the unknown. Soil Biol Biochem 63:18–23CrossRefGoogle Scholar
  30. Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner J, Amelung W, Grohmann E, Siemens J (2012) Accumulation of pharmaceuticals, Enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in central Mexico. PLoS One 7(9):e45397PubMedPubMedCentralCrossRefGoogle Scholar
  31. Da Silva MF, Tiago I, Veríssimo A, Boaventura RA, Nunes OC, Manaia CM (2006) Antibiotic resistance of enterococci and related bacteria in an urban wastewater treatment plant. FEMS Microbiol Ecol 55(2):322–329CrossRefGoogle Scholar
  32. D’costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311(5759):374–377PubMedCrossRefGoogle Scholar
  33. D’Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R (2011) Antibiotic resistance is ancient. Nature 477(7365):457–461PubMedCrossRefGoogle Scholar
  34. Deering AJ, Mauer LJ, Pruitt RE (2012) Internalization of E. coli O157: H7 and Salmonella spp. in plants: a review. Food Res Int 45(2):567–575CrossRefGoogle Scholar
  35. DeFlaun MF, Paul JH (1989) Detection of exogenous gene sequences in dissolved DNA from aquatic environments. Microb Ecol 18(1):21–28PubMedCrossRefGoogle Scholar
  36. Denis C, Poirel L, Carricajo A, Grattard F, Fascia P, Verhoeven P, Gay P, Nuti C, Nordmann P, Pozzetto B (2012) Nosocomial transmission of NDM-1-producing Escherichia coli within a non-endemic area in France. Clin Microbiol Infect 18(5):E128–E130PubMedCrossRefGoogle Scholar
  37. de Vries J, Meier P, Wackernagel W (2001) The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiol Lett 195(2):211–215PubMedCrossRefGoogle Scholar
  38. Djordjevic SP, Stokes HW, Roy Chowdhury P (2013) Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front Microbiol 4:86PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dominiak DM, Nielsen JL, Nielsen PH (2011) Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 13(3):710–721PubMedCrossRefGoogle Scholar
  40. Dortet L (2012) New Delhi Metallo-β-Lactamase 4-producing Escherichia coli in Cameroon. Emerg Infect Dis 18(9):1540PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dunlop P, Ciavola M, Rizzo L, Byrne J (2011) Inactivation and injury assessment of Escherichia coli during solar and photocatalytic disinfection in LDPE bags. Chemosphere 85(7):1160–1166PubMedCrossRefGoogle Scholar
  42. Eisenstark A (1987) Mutagenic and lethal effects of near-ultraviolet radiation (290-400 nm) on bacteria and phage. Environ Mol Mutagen 10(3):317–337PubMedCrossRefGoogle Scholar
  43. Espinosa-Urgel M (2004) Plant-associated Pseudomonas populations: molecular biology, DNA dynamics, and gene transfer. Plasmid 52(3):139–150PubMedCrossRefGoogle Scholar
  44. Fahrenfeld NL, Ma Y, O’Brien M, Pruden A (2013) Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Front Microbiol 4:130PubMedPubMedCentralCrossRefGoogle Scholar
  45. Feil EJ, Spratt BG (2001) Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55(1):561–590PubMedCrossRefGoogle Scholar
  46. Fernandez-Astorga A, Muela A, Cisterna R, Iriberri J, Barcina I (1992) Biotic and abiotic factors affecting plasmid transfer in Escherichia coli strains. Appl Environ Microbiol 58(1):392–398PubMedPubMedCentralGoogle Scholar
  47. Ferro G, Guarino F, Cicatelli A, Rizzo L (2017) β-lactams resistance gene quantification in an antibiotic resistant Escherichia coli water suspension treated by advanced oxidation with UV/H 2 O 2. J Hazard Mater 323:426–433PubMedCrossRefGoogle Scholar
  48. Fiett J, Baraniak A, Izdebski R, Sitkiewicz I, Zabicka D, Meler A, Filczak K, Hryniewicz W, Gniadkowski M (2014) The first NDM metallo-beta-lactamase-producing Enterobacteriaceae isolate in Poland: evolution of IncFII-type plasmids carrying the bla(NDM-1) gene. Antimicrob Agents Chemother 58(2):1203–1207PubMedPubMedCentralCrossRefGoogle Scholar
  49. Fisher MB, Keenan CR, Nelson KL, Voelker BM (2008) Speeding up solar disinfection (SODIS): effects of hydrogen peroxide, temperature, pH, and copper plus ascorbate on the photoinactivation of E. coli. J Water Health 6(1):35–51PubMedCrossRefGoogle Scholar
  50. Fisher MB, Iriarte M, Nelson KL (2012) Solar water disinfection (SODIS) of Escherichia coli, Enterococcus spp., and MS2 coliphage: effects of additives and alternative container materials. Water Res 46(6):1745–1754PubMedCrossRefGoogle Scholar
  51. Fouts DE, Tyler HL, DeBoy RT, Daugherty S, Ren Q, Badger JH, Durkin AS, Huot H, Shrivastava S, Kothari S (2008) Complete genome sequence of the N 2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4(7):e1000141PubMedPubMedCentralCrossRefGoogle Scholar
  52. Goldman G, Starosvetsky J, Armon R (2009) Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. J Membr Sci 342(1):145–152CrossRefGoogle Scholar
  53. Gomes C, Da Silva P, Moreira RG, Castell-Perez E, Ellis EA, Pendleton M (2009) Understanding E. coli internalization in lettuce leaves for optimization of irradiation treatment. Int J Food Microbiol 135(3):238–247PubMedCrossRefGoogle Scholar
  54. Goodsell DS (2001) The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 6(3):298–299PubMedCrossRefGoogle Scholar
  55. Götz A, Pukall R, Smit E, Tietze E, Prager R, Tschäpe H, Van Elsas J, Smalla K (1996) Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl Environ Microbiol 62(7):2621–2628PubMedPubMedCentralGoogle Scholar
  56. Guo M-T, Yuan Q-B, Yang J (2013) Ultraviolet reduction of erythromycin and tetracycline resistant heterotrophic bacteria and their resistance genes in municipal wastewater. Chemosphere 93(11):2864–2868PubMedCrossRefGoogle Scholar
  57. Halaby T, Reuland AE, Al Naiemi N, Potron A, Savelkoul PH, Vandenbroucke-Grauls CM, Nordmann P (2012) A case of New Delhi metallo-beta-lactamase 1 (NDM-1)-producing Klebsiella pneumoniae with putative secondary transmission from the Balkan region in the Netherlands. Antimicrob Agents Chemother 56(5):2790–2791PubMedPubMedCentralCrossRefGoogle Scholar
  58. Harb M, Hong P-Y (2016) Molecular-based detection of potentially pathogenic bacteria in membrane bioreactor (MBR) systems treating municipal wastewater: a case study. Environ Sci Pollut Res 24(6):5370–5380CrossRefGoogle Scholar
  59. Heuer H, Smalla K (2007) Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ Microbiol 9(3):657–666PubMedCrossRefGoogle Scholar
  60. Heuer H, Solehati Q, Zimmerling U, Kleineidam K, Schloter M, Müller T, Focks A, Thiele-Bruhn S, Smalla K (2011) Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl Environ Microbiol 77(7):2527–2530PubMedPubMedCentralCrossRefGoogle Scholar
  61. Ho PL, Lo WU, Yeung MK, Lin CH, Chow KH, Ang I, Tong AH, Bao JY, Lok S, Lo JY (2011) Complete sequencing of pNDM-HK encoding NDM-1 carbapenemase from a multidrug-resistant Escherichia coli strain isolated in Hong Kong. PLoS One 6(3):e17989PubMedPubMedCentralCrossRefGoogle Scholar
  62. Ho PL, Li Z, Lai EL, Chiu SS, Cheng VC (2012) Emergence of NDM-1-producing Enterobacteriaceae in China. J Antimicrob Chemother 67(6):1553–1555PubMedCrossRefGoogle Scholar
  63. Hofreiter M, Serre D, Poinar HN, Kuch M, Pääbo S (2001) Ancient DNA. Nat Rev Genet 2(5):353–359PubMedCrossRefGoogle Scholar
  64. Holden N, Pritchard L, Toth I (2009) Colonization outwith the colon: plants as an alternative environmental reservoir for human pathogenic enterobacteria. FEMS Microbiol Rev 33(4):689–703PubMedCrossRefGoogle Scholar
  65. Hong P-Y, Yannarell AC, Dai Q, Ekizoglu M, Mackie RI (2013) Monitoring the perturbation of soil and groundwater microbial communities due to pig production activities. Appl Environ Microbiol 79(8):2620–2629PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hornsey M, Phee L, Wareham DW (2011) A novel variant, NDM-5, of the New Delhi metallo-beta-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother 55(12):5952–5954PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hughes VM, Datta N (1983) Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302(5910):725–726PubMedCrossRefGoogle Scholar
  68. Ikeda H, Shiraishi K, Ogata Y (2004) Illegitimate recombination mediated by double-strand break and end-joining in Escherichia coli. Adv Biophys 38:3–20CrossRefGoogle Scholar
  69. Islam M, Morgan J, Doyle MP, Jiang X (2004) Fate of Escherichia coli O157: H7 in manure compost-amended soil and on carrots and onions grown in an environmentally controlled growth chamber. J Food Prot 67(3):574–578PubMedCrossRefGoogle Scholar
  70. Isozumi R, Yoshimatsu K, Yamashiro T, Hasebe F, Nguyen BM, Ngo TC, Yasuda SP, Koma T, Shimizu K, Arikawa J (2012) bla(NDM-1)-positive Klebsiella pneumoniae from environment, Vietnam. Emerg Infect Dis 18(8):1383–1385PubMedPubMedCentralCrossRefGoogle Scholar
  71. Itoh Y, Sugita-Konishi Y, Kasuga F, Iwaki M, Hara-Kudo Y, Saito N, Noguchi Y, Konuma H, Kumagai S (1998) Enterohemorrhagic Escherichia coli O157: H7 present in radish sprouts. Appl Environ Microbiol 64(4):1532–1535PubMedPubMedCentralGoogle Scholar
  72. Jagger J (1981) Near-UV radiation effects on microorganisms. Photochem Photobiol 34(6):761–768PubMedCrossRefGoogle Scholar
  73. Jassim SA, Limoges RG (2014) Natural solution to antibiotic resistance: bacteriophages ‘The Living Drugs’. World J Microbiol Biotechnol 30(8):2153–2170PubMedPubMedCentralCrossRefGoogle Scholar
  74. Jassim SA, Limoges RG, El-Cheikh H (2016) Bacteriophage biocontrol in wastewater treatment. World J Microbiol Biotechnol 32(4):1–10CrossRefGoogle Scholar
  75. Johnson AP, Woodford N (2013) Global spread of antibiotic resistance: the example of New Delhi metallo-beta-lactamase (NDM)-mediated carbapenem resistance. J Med Microbiol 62(Pt 4):499–513PubMedCrossRefGoogle Scholar
  76. Jones JB, Vallad GE, Iriarte FB, Obradović A, Wernsing MH, Jackson LE, Balogh B, Hong JC, Momol MT (2012) Considerations for using bacteriophages for plant disease control. Bacteriophage 2(4):e23857CrossRefGoogle Scholar
  77. Jones LA, Worobo RW, Smart CD (2014) UV light inactivation of human and plant pathogens in unfiltered surface irrigation water. Appl Environ Microbiol 80(3):849–854PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kaase M, Nordmann P, Wichelhaus TA, Gatermann SG, Bonnin RA, Poirel L (2011) NDM-2 carbapenemase in Acinetobacter baumannii from Egypt. J Antimicrob Chemother 66(6):1260–1262PubMedCrossRefGoogle Scholar
  79. Karl DM, Bailiff MD (1989) The measurement and distribution of dissolved nucleic acids in aquatic environments. Limnol Oceanogr 34(3):543–558CrossRefGoogle Scholar
  80. Khaengraeng R, Reed RH (2005) Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol 99(1):39–50PubMedCrossRefGoogle Scholar
  81. Khairnar K, Pal P, Chandekar RH, Paunikar WN (2014) Isolation and characterization of bacteriophages infecting nocardioforms in wastewater treatment plant. Biotechnol Res Int 2014:151952PubMedPubMedCentralCrossRefGoogle Scholar
  82. Khan M, Satoh H, Mino T, Katayama H, Kurisu F, Matsuo T (2002a) Bacteriophage-host interaction in the enhanced biological phosphate removing activated sludge system. Water Sci Technol 46(1–2):39–43PubMedGoogle Scholar
  83. Khan MA, Satoh H, Katayama H, Kurisu F, Mino T (2002b) Bacteriophages isolated from activated sludge processes and their polyvalency. Water Res 36(13):3364–3370PubMedCrossRefGoogle Scholar
  84. Kim MN, Yong D, An D, Chung HS, Woo JH, Lee K, Chong Y (2012) Nosocomial clustering of NDM-1-producing Klebsiella pneumoniae sequence type 340 strains in four patients at a South Korean tertiary care hospital. J Clin Microbiol 50(4):1433–1436PubMedPubMedCentralCrossRefGoogle Scholar
  85. King D, Strynadka N (2011) Crystal structure of New Delhi metallo-beta-lactamase reveals molecular basis for antibiotic resistance. Protein Sci 20(9):1484–1491PubMedPubMedCentralCrossRefGoogle Scholar
  86. Knapp CW, Dolfing J, Ehlert PA, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44(2):580–587PubMedCrossRefGoogle Scholar
  87. Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, Granot D, Sela S (2009) Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl Environ Microbiol 75(19):6076–6086PubMedPubMedCentralCrossRefGoogle Scholar
  88. Kumarasamy K, Kalyanasundaram A (2012) Emergence of Klebsiella pneumoniae isolate co-producing NDM-1 with KPC-2 from India. J Antimicrob Chemother 67(1):243–244PubMedCrossRefGoogle Scholar
  89. Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10(9):597–602PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lai CC, Lin TL, Tseng SP, Huang YT, Wang JT, Chang SC, Teng LJ, Wang JT, Hsueh PR (2011) Pelvic abscess caused by New Delhi metallo-beta-lactamase-1-producing Klebsiella oxytoca in Taiwan in a patient who underwent renal transplantation in China. Diagn Microbiol Infect Dis 71(4):474–475PubMedCrossRefGoogle Scholar
  91. Le T-H, Ng C, Chen H, Yi XZ, Koh TH, Barkham TMS, Zhou Z, Gin KY-H (2016) Occurrences and characterization of antibiotic-resistant bacteria and genetic determinants of hospital wastewater in a tropical country. Antimicrob Agents Chemother 60(12):7449–7456PubMedPubMedCentralGoogle Scholar
  92. Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Dunfield KE (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39(12):2977–2991CrossRefGoogle Scholar
  93. Lilley AK, Fry JC, Day MJ, Bailey MJ (1994) In situ transfer of an exogenously isolated plasmid between Pseudomonas spp. in sugar beet rhizosphere. Microbiology 140(1):27–33CrossRefGoogle Scholar
  94. Lloyd RE, Rinkenberger JL, Hug BA, Tuveson RW (1990) Growing Escherichia coli mutants deficient in riboflavin biosynthesis with non-limiting riboflavin results in sensitization to inactivation by broad-spectrum near-ultraviolet light (320-400 nm). Photochem Photobiol 52(4):897–901PubMedCrossRefGoogle Scholar
  95. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58(3):563–602PubMedPubMedCentralGoogle Scholar
  96. Luo Y, Yang F, Mathieu J, Mao D, Wang Q, Alvarez P (2013) Proliferation of multidrug-resistant New Delhi metallo-β-lactamase genes in municipal wastewater treatment plants in northern China. Environ Sci Technol Lett 1(1):26–30CrossRefGoogle Scholar
  97. Majewski J, Cohan FM (1998) The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148(1):13–18PubMedPubMedCentralGoogle Scholar
  98. Majewski J, Zawadzki P, Pickerill P, Cohan FM, Dowson CG (2000) Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J Bacteriol 182(4):1016–1023PubMedPubMedCentralCrossRefGoogle Scholar
  99. Malato S, Fernández-Ibáñez P, Maldonado M, Blanco J, Gernjak W (2009) Decontamination and disinfection of water by solar photocatalysis: recent overview and trends. Catal Today 147(1):1–59CrossRefGoogle Scholar
  100. Mantilla-Calderon D, Jumat MR, Wang T, Ganesan P, Al-Jassim N, Hong P-Y (2016) Isolation and characterization of NDM-positive Escherichia coli from municipal wastewater in Jeddah, Saudi Arabia. Antimicrob Agents Chemother 60(9):5223–5231PubMedPubMedCentralCrossRefGoogle Scholar
  101. Marti R, Scott A, Tien Y-C, Murray R, Sabourin L, Zhang Y, Topp E (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(18):5701–5709PubMedPubMedCentralCrossRefGoogle Scholar
  102. Mason KA, Losos JB, Singer SR, Peter H (2011) Biology. McGraw-Hill, New York, p 533Google Scholar
  103. Matic I, Radman M, Taddei F, Picard B, Doit C, Bingen E, Denamur E, Elion J (1997) Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277(5333):1833–1834PubMedCrossRefGoogle Scholar
  104. Mazzariol A, Bosnjak Z, Ballarini P, Budimir A, Bedenic B, Kalenic S, Cornaglia G (2012) NDM-1-producing Klebsiella pneumoniae, Croatia. Emerg Infect Dis 18(3):532–534PubMedPubMedCentralCrossRefGoogle Scholar
  105. McGann P, Hang J, Clifford RJ, Yang Y, Kwak YI, Kuschner RA, Lesho EP, Waterman PE (2012) Complete sequence of a novel 178-kilobase plasmid carrying bla(NDM-1) in a Providencia stuartii strain isolated in Afghanistan. Antimicrob Agents Chemother 56(4):1673–1679PubMedCrossRefGoogle Scholar
  106. McGuigan KG, Joyce TM, Conroy RM, Gillespie JB, Elmore-Meegan M (1998) Solar disinfection of drinking water contained in transparent plastic bottles: characterizing the bacterial inactivation process. J Appl Microbiol 84(6):1138–1148PubMedCrossRefGoogle Scholar
  107. McGuigan KG, Conroy RM, Mosler HJ, du Preez M, Ubomba-Jaswa E, Fernandez-Ibanez P (2012) Solar water disinfection (SODIS): a review from bench-top to roof-top. J Hazard Mater 235–236:29–46PubMedCrossRefGoogle Scholar
  108. McKinney CW, Pruden A (2012) Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ Sci Technol 46(24):13393–13400PubMedCrossRefGoogle Scholar
  109. Méjean V, Claverys J-P (1993) DNA processing during entry in transformation of Streptococcus pneumoniae. J Biol Chem 268(8):5594–5599PubMedGoogle Scholar
  110. Miriagou V, Cornaglia G, Edelstein M, Galani I, Giske C, Gniadkowski M, Malamou-Lada E, Martinez-Martinez L, Navarro F, Nordmann P (2010) Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clin Microbiol Infect 16(2):112–122PubMedCrossRefGoogle Scholar
  111. Morris CE, Monier J-M (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41(1):429–453PubMedCrossRefGoogle Scholar
  112. Muela A, Garcia-Bringas JM, Seco C, Arana I, Barcina I (2002) Participation of oxygen and role of exogenous and endogenous sensitizers in the photoinactivation of Escherichia coli by photosynthetically active radiation, UV-A and UV-B. Microb Ecol 44(4):354–364PubMedCrossRefGoogle Scholar
  113. Mulvey MR, Grant JM, Plewes K, Roscoe D, Boyd DA (2011) New Delhi metallo-beta-lactamase in Klebsiella pneumoniae and Escherichia coli, Canada. Emerg Infect Dis 17(1):103–106PubMedPubMedCentralCrossRefGoogle Scholar
  114. Munir M, Xagoraraki I (2011) Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J Environ Qual 40(1):248–255PubMedCrossRefGoogle Scholar
  115. Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45(2):681–693PubMedCrossRefGoogle Scholar
  116. Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012) Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ Sci Technol 46(9):4800–4808PubMedCrossRefGoogle Scholar
  117. Nesme J, Simonet P (2015) The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ Microbiol 17(4):913–930PubMedCrossRefGoogle Scholar
  118. Nielsen KM, Bones AM, Van Elsas J (1997a) Induced natural transformation of Acinetobacter calcoaceticus in soil microcosms. Appl Environ Microbiol 63(10):3972–3977PubMedPubMedCentralGoogle Scholar
  119. Nielsen KM, Van Weerelt M, Berg TN, Bones AM, Hagler AN, Van Elsas J (1997b) Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms. Appl Environ Microbiol 63(5):1945–1952PubMedPubMedCentralGoogle Scholar
  120. Nielsen KM, van Elsas JD, Smalla K (2000) Transformation of Acinetobacter sp. strain BD413 (pFG4ΔnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl Environ Microbiol 66(3):1237–1242PubMedPubMedCentralCrossRefGoogle Scholar
  121. Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D (2007) Release and persistence of extracellular DNA in the environment. Environ Biosaf Res 6(1–2):37–53CrossRefGoogle Scholar
  122. Nielsen JB, Hansen F, Littauer P, Schonning K, Hammerum AM (2012) An NDM-1-producing Escherichia coli obtained in Denmark has a genetic profile similar to an NDM-1-producing E. coli isolate from the UK. J Antimicrob Chemother 67(8):2049–2051PubMedCrossRefGoogle Scholar
  123. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2-3):313–339PubMedCrossRefGoogle Scholar
  124. Nordmann P, Boulanger AE, Poirel L (2012) NDM-4 metallo-beta-lactamase with increased carbapenemase activity from Escherichia coli. Antimicrob Agents Chemother 56(4):2184–2186PubMedPubMedCentralCrossRefGoogle Scholar
  125. Novais Â, Cantón R, Moreira R, Peixe L, Baquero F, Coque TM (2007) Emergence and dissemination of Enterobacteriaceae isolates producing CTX-M-1-like enzymes in Spain are associated with IncFII (CTX-M-15) and broad-host-range (CTX-M-1,-3, and-32) plasmids. Antimicrob Agents Chemother 51(2):796–799PubMedCrossRefGoogle Scholar
  126. Oates PM, Shanahan P, Polz MF (2003) Solar disinfection (SODIS): simulation of solar radiation for global assessment and application for point-of-use water treatment in Haiti. Water Res 37(1):47–54PubMedCrossRefGoogle Scholar
  127. Ogram A, Sayler GS, Barkay T (1987) The extraction and purification of microbial DNA from sediments. J Microbiol Methods 7(2–3):57–66CrossRefGoogle Scholar
  128. Oteo J, Domingo-Garcia D, Fernandez-Romero S, Saez D, Guiu A, Cuevas O, Lopez-Brea M, Campos J (2012) Abdominal abscess due to NDM-1-producing Klebsiella pneumoniae in Spain. J Med Microbiol 61(Pt 6):864–867PubMedCrossRefGoogle Scholar
  129. Pal P, Khairnar K, Paunikar W (2014) Causes and remedies for filamentous foaming in activated sludge treatment plant. Global NEST J 16(4):762–772Google Scholar
  130. Palmen R, Hellingwerf KJ (1997) Uptake and processing of DNA by Acinetobacter calcoaceticus—a review. Gene 192(1):179–190PubMedCrossRefGoogle Scholar
  131. Pasteran F, Albornoz E, Faccone D, Gomez S, Valenzuela C, Morales M, Estrada P, Valenzuela L, Matheu J, Guerriero L, Arbizu E, Calderon Y, Ramon-Pardo P, Corso A (2012) Emergence of NDM-1-producing Klebsiella pneumoniae in Guatemala. J Antimicrob Chemother 67(7):1795–1797PubMedCrossRefGoogle Scholar
  132. Pattison DI, Davies MJ (2006) Actions of ultraviolet light on cellular structures. In: Bignold LP (ed) Cancer: cell structures, carcinogens and genomic instability, vol 96. Birkhäuser, Basel, pp 131–157CrossRefGoogle Scholar
  133. Peirano G, Ahmed-Bentley J, Woodford N, Pitout JD (2011a) New Delhi metallo-beta-lactamase from traveler returning to Canada. Emerg Infect Dis 17(2):242–244PubMedPubMedCentralCrossRefGoogle Scholar
  134. Peirano G, Pillai DR, Pitondo-Silva A, Richardson D, Pitout JD (2011b) The characteristics of NDM-producing Klebsiella pneumoniae from Canada. Diagn Microbiol Infect Dis 71(2):106–109PubMedCrossRefGoogle Scholar
  135. Petrovski S, Seviour RJ, Tillett D (2011a) Characterization of the genome of the polyvalent lytic bacteriophage GTE2, which has potential for biocontrol of Gordonia-, Rhodococcus-, and Nocardia-stabilized foams in activated sludge plants. Appl Environ Microbiol 77(12):3923–3929PubMedPubMedCentralCrossRefGoogle Scholar
  136. Petrovski S, Seviour RJ, Tillett D (2011b) Prevention of Gordonia and Nocardia stabilized foam formation by using bacteriophage GTE7. Appl Environ Microbiol 77(21):7864–7867PubMedPubMedCentralCrossRefGoogle Scholar
  137. Pfeifer GP (1997) Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochem Photobiol 65(2):270–283PubMedCrossRefGoogle Scholar
  138. Piepersberg W, Distler J, Heinzel P, Perez-Gonzalez J-A (1988) Antibiotic resistance by modification: many resistance genes could be derived from cellular control genes in actinomycetes-A hypothesis. Actinomycetologica 2(2):83–98CrossRefGoogle Scholar
  139. Poirel L, Hombrouck-Alet C, Freneaux C, Bernabeu S, Nordmann P (2010a) Global spread of New Delhi metallo-β-lactamase 1. Lancet Infect Dis 10(12):832PubMedCrossRefGoogle Scholar
  140. Poirel L, Lagrutta E, Taylor P, Pham J, Nordmann P (2010b) Emergence of metallo-beta-lactamase NDM-1-producing multidrug-resistant Escherichia coli in Australia. Antimicrob Agents Chemother 54(11):4914–4916PubMedPubMedCentralCrossRefGoogle Scholar
  141. Poirel L, Al Maskari Z, Al Rashdi F, Bernabeu S, Nordmann P (2011a) NDM-1-producing Klebsiella pneumoniae isolated in the Sultanate of Oman. J Antimicrob Chemother 66(2):304–306PubMedCrossRefGoogle Scholar
  142. Poirel L, Benouda A, Hays C, Nordmann P (2011b) Emergence of NDM-1-producing Klebsiella pneumoniae in Morocco. J Antimicrob Chemother 66(12):2781–2783PubMedCrossRefGoogle Scholar
  143. Poirel L, Dortet L, Bernabeu S, Nordmann P (2011c) Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother 55(11):5403–5407PubMedPubMedCentralCrossRefGoogle Scholar
  144. Poirel L, Fortineau N, Nordmann P (2011d) International transfer of NDM-1-producing Klebsiella pneumoniae from Iraq to France. Antimicrob Agents Chemother 55(4):1821–1822PubMedPubMedCentralCrossRefGoogle Scholar
  145. Poirel L, Revathi G, Bernabeu S, Nordmann P (2011e) Detection of NDM-1-producing Klebsiella pneumoniae in Kenya. Antimicrob Agents Chemother 55(2):934–936PubMedCrossRefGoogle Scholar
  146. Poirel L, Ros A, Carricajo A, Berthelot P, Pozzetto B, Bernabeu S, Nordmann P (2011f) Extremely drug-resistant Citrobacter freundii isolate producing NDM-1 and other carbapenemases identified in a patient returning from India. Antimicrob Agents Chemother 55(1):447–448PubMedCrossRefGoogle Scholar
  147. Poirel L, Schrenzel J, Cherkaoui A, Bernabeu S, Renzi G, Nordmann P (2011g) Molecular analysis of NDM-1-producing enterobacterial isolates from Geneva, Switzerland. J Antimicrob Chemother 66(8):1730–1733PubMedCrossRefGoogle Scholar
  148. Poirel L, Lascols C, Bernabeu S, Nordmann P (2012a) NDM-1-producing Klebsiella pneumoniae in Mauritius. Antimicrob Agents Chemother 56(1):598–599PubMedPubMedCentralCrossRefGoogle Scholar
  149. Poirel L, Ozdamar M, Ocampo-Sosa AA, Turkoglu S, Ozer UG, Nordmann P (2012b) NDM-1-producing Klebsiella pneumoniae now in Turkey. Antimicrob Agents Chemother 56(5):2784–2785PubMedPubMedCentralCrossRefGoogle Scholar
  150. Poole K (2005) Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56(1):20–51PubMedCrossRefGoogle Scholar
  151. Pruden A, Larsson DJ, Amézquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JM, Suzuki S, Silley P, Snape JR (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121(8):878PubMedPubMedCentralCrossRefGoogle Scholar
  152. Rahme LG, Stevens EJ, Wolfort SF, Shao J (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268(5219):1899PubMedCrossRefGoogle Scholar
  153. Rahube TO, Marti R, Scott A, Tien Y-C, Murray R, Sabourin L, Zhang Y, Duenk P, Lapen DR, Topp E (2014) Impact of fertilizing with raw or anaerobically digested sewage sludge on the abundance of antibiotic-resistant coliforms, antibiotic resistance genes, and pathogenic bacteria in soil and on vegetables at harvest. Appl Environ Microbiol 80(22):6898–6907PubMedPubMedCentralCrossRefGoogle Scholar
  154. Raynaud X, Nunan N (2014) Spatial ecology of bacteria at the microscale in soil. PLoS One 9(1):e87217PubMedPubMedCentralCrossRefGoogle Scholar
  155. Riesenfeld CS, Goodman RM, Handelsman J (2004) Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ Microbiol 6(9):981–989PubMedCrossRefGoogle Scholar
  156. Rijal GK, Fujioka RS (2003) Use of reflectors to enhance the synergistic effects of solar heating and solar wavelengths to disinfect drinking water sources. Water Sci Technol 48(11-12):481–488PubMedGoogle Scholar
  157. Rizzo L, Fiorentino A, Anselmo A (2012) Effect of solar radiation on multidrug resistant E. coli strains and antibiotic mixture photodegradation in wastewater polluted stream. Sci Total Environ 427:263–268PubMedCrossRefGoogle Scholar
  158. Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360PubMedCrossRefGoogle Scholar
  159. Santos AL, Gomes NC, Henriques I, Almeida A, Correia A, Cunha A (2012) Contribution of reactive oxygen species to UV-B-induced damage in bacteria. J Photochem Photobiol B Biol 117:40–46CrossRefGoogle Scholar
  160. Schlüter 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(4):449–477PubMedCrossRefGoogle Scholar
  161. Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43(3):325–335PubMedCrossRefGoogle Scholar
  162. Segawa T, Takeuchi N, Rivera A, Yamada A, Yoshimura Y, Barcaza G, Shinbori K, Motoyama H, Kohshima S, Ushida K (2013) Distribution of antibiotic resistance genes in glacier environments. Environ Microbiol Rep 5(1):127–134PubMedCrossRefGoogle Scholar
  163. Sekizuka T, Matsui M, Yamane K, Takeuchi F, Ohnishi M, Hishinuma A, Arakawa Y, Kuroda M (2011) Complete sequencing of the bla(NDM-1)-positive IncA/C plasmid from Escherichia coli ST38 isolate suggests a possible origin from plant pathogens. PLoS One 6(9):e25334PubMedPubMedCentralCrossRefGoogle Scholar
  164. Selenska S, Klingmüller W (1992) Direct recovery and molecular analysis of DNA and RNA from soil. Microb Releases 1(1):41–46PubMedGoogle Scholar
  165. Sidjabat H, Nimmo GR, Walsh TR, Binotto E, Htin A, Hayashi Y, Li J, Nation RL, George N, Paterson DL (2011) Carbapenem resistance in Klebsiella pneumoniae due to the New Delhi Metallo-beta-lactamase. Clin Infect Dis 52(4):481–484PubMedPubMedCentralCrossRefGoogle Scholar
  166. Sinton LW, Hall CH, Lynch PA, Davies-Colley RJ (2002) Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl Environ Microbiol 68(3):1122–1131PubMedPubMedCentralCrossRefGoogle Scholar
  167. Smith DH (1967) R factor infection of Escherichia coli lyophilized in 1946. J Bacteriol 94(6):2071PubMedPubMedCentralGoogle Scholar
  168. Sole M, Pitart C, Roca I, Fabrega A, Salvador P, Munoz L, Oliveira I, Gascon J, Marco F, Vila J (2011) First description of an Escherichia coli strain producing NDM-1 carbapenemase in Spain. Antimicrob Agents Chemother 55(9):4402–4404PubMedPubMedCentralCrossRefGoogle Scholar
  169. Solomon EB, Yaron S, Matthews KR (2002) Transmission of Escherichia coli O157: H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl Environ Microbiol 68(1):397–400PubMedPubMedCentralCrossRefGoogle Scholar
  170. Sommer B, Marino A, Solarte Y, Salas M, Dierolf C, Valiente C, Mora D, Rechsteiner R, Setter P, Wirojanagud W (1997) SODIS—an emerging water treatment process. Aqua (Oxford) 46(3):127–137Google Scholar
  171. Sørensen SJ, Jensen LE (1998) Transfer of plasmid RP4 in the spermosphere and rhizosphere of barley seedling. Antonie Van Leeuwenhoek 73(1):69–77PubMedCrossRefGoogle Scholar
  172. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE (2001) Common and contrasting themes of plant and animal diseases. Science 292(5525):2285–2289PubMedCrossRefGoogle Scholar
  173. Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol Rev 35(5):790–819PubMedCrossRefGoogle Scholar
  174. Sulakvelidze A, Alavidze Z, Morris JG (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45(3):649–659PubMedPubMedCentralCrossRefGoogle Scholar
  175. Suzuki H, Yano H, Brown CJ, Top EM (2010) Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192(22):6045–6055PubMedPubMedCentralCrossRefGoogle Scholar
  176. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3(9):711–721PubMedCrossRefGoogle Scholar
  177. Thomas J, Soddell JA, Kurtböke D (2002) Fighting foam with phages? Water Sci Technol 46(1–2):511–518PubMedGoogle Scholar
  178. Tijet N (2011) New Delhi metallo-β-lactamase, Ontario, Canada. Emerg Infect Dis 17(2):306PubMedPubMedCentralCrossRefGoogle Scholar
  179. Toth IK, Pritchard L, Birch PR (2006) Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu Rev Phytopathol 44:305–336PubMedCrossRefGoogle Scholar
  180. Ubomba-Jaswa E, Navntoft C, Polo-Lopez MI, Fernandez-Ibanez P, McGuigan KG (2009) Solar disinfection of drinking water (SODIS): an investigation of the effect of UV-A dose on inactivation efficiency. Photochem Photobiol Sci 8(5):587–595PubMedCrossRefGoogle Scholar
  181. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci USA 111(42):15202–15207PubMedPubMedCentralCrossRefGoogle Scholar
  182. USEPA (2006) Ultraviolet disinfection guidance manual for the final long term 2 enhanced surface water treatment rule. Date last accessed 4 May 2017
  183. Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014) Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14(8):742–750PubMedCrossRefGoogle Scholar
  184. Van Elsas JD, Bailey MJ (2002) The ecology of transfer of mobile genetic elements. FEMS Microbiol Ecol 42(2):187–197PubMedCrossRefGoogle Scholar
  185. Van Elsas J, Fry J, Hirsch P, Molin S (2000) Ecology of plasmid transfer and spread. In: Thomas CM (ed) The horizontal gene pool; Bacterial plasmids and gene spread. Harwood, Amsterdam, pp 175–206Google Scholar
  186. Vulić M, Dionisio F, Taddei F, Radman M (1997) Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc Natl Acad Sci USA 94(18):9763–9767PubMedPubMedCentralCrossRefGoogle Scholar
  187. Walsh TR, Weeks J, Livermore DM, Toleman MA (2011) Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 11(5):355–362PubMedCrossRefGoogle Scholar
  188. Walther-Rasmussen J, Høiby N (2007) Class A carbapenemases. J Antimicrob Chemother 60(3):470–482PubMedCrossRefGoogle Scholar
  189. Wang Z, Fast W, Valentine AM, Benkovic SJ (1999) Metallo-β-lactamase: structure and mechanism. Curr Opin Chem Biol 3(5):614–622PubMedCrossRefGoogle Scholar
  190. Wang F, Stedtfeld RD, Kim O-S, Chai B, Yang L, Stedtfeld TM, Hong SG, Kim D, Lim HS, Hashsham SA (2016) Influence of soil characteristics and proximity to antarctic research stations on abundance of antibiotic resistance genes in soils. Environ Sci Technol 50(23):12621–12629PubMedCrossRefGoogle Scholar
  191. Webb RB, Brown MS (1979) Action spectra for oxygen-dependent and independent inactivation of Escherichia coli WP2s from 254 to 460 nm. Photochem Photobiol 29(2):407–409PubMedCrossRefGoogle Scholar
  192. Wegelin M, Canonica S, Mechsner K, Fleischmann T, Pesaro F, Metzler A (1994) Solar water disinfection: scope of the process and analysis of radiation experiments. Aqua 43(4):154–169Google Scholar
  193. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181PubMedCrossRefGoogle Scholar
  194. Williamson DA, Sidjabat HE, Freeman JT, Roberts SA, Silvey A, Woodhouse R, Mowat E, Dyet K, Paterson DL, Blackmore T, Burns A, Heffernan H (2012) Identification and molecular characterisation of New Delhi metallo-beta-lactamase-1 (NDM-1)- and NDM-6-producing Enterobacteriaceae from New Zealand hospitals. Int J Antimicrob Agents 39(6):529–533PubMedCrossRefGoogle Scholar
  195. Withey S, Cartmell E, Avery L, Stephenson T (2005) Bacteriophages—potential for application in wastewater treatment processes. Sci Total Environ 339(1):1–18PubMedCrossRefGoogle Scholar
  196. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5(3):175–186PubMedCrossRefGoogle Scholar
  197. Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR (2009) Characterization of a new metallo-β-lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 53(12):5046–5054PubMedPubMedCentralCrossRefGoogle Scholar
  198. Yosef I, Manor M, Kiro R, Qimron U (2015) Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc Natl Acad Sci USA 112(23):7267–7272PubMedPubMedCentralCrossRefGoogle Scholar
  199. Zhang Y, Zhuang Y, Geng J, Ren H, Zhang Y, Ding L, Xu K (2015) Inactivation of antibiotic resistance genes in municipal wastewater effluent by chlorination and sequential UV/chlorination disinfection. Sci Total Environ 512:125–132PubMedCrossRefGoogle Scholar
  200. Zhang Y, Zhuang Y, Geng J, Ren H, Xu K, Ding L (2016) Reduction of antibiotic resistance genes in municipal wastewater effluent by advanced oxidation processes. Sci Total Environ 550:184–191PubMedCrossRefGoogle Scholar
  201. Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110(9):3435–3440PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Biological and Environmental Science & Engineering Division (BESE)King Abdullah University of Science and Technology (KAUST)ThuwalSaudi Arabia
  2. 2.Water Desalination and Reuse Center (WDRC)King Abdullah University of Science and Technology (KAUST)ThuwalSaudi Arabia

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