Removal of intl1 and associated antibiotics resistant genes in water, sewage sludge and livestock manure treatments

review paper

Abstract

Antibiotics resistant genes (ARGs) are frequently detected in different media, such as wastewater, sewage sludge, and livestock manure. ARGs have been evidenced to have more and more threats to our environment because of their increase in species and total abundances causing more attention especially in horizontal gene transfer (HGT). The integron, an important form of mobile gene elements transfer ARGs through HGT, is demonstrated to have a high risk to human beings, and the class 1 integron (intl1), a predominant integron, is a marker of the process of horizontal gene transfer. Tetracycline, sulfonamides, macrolide, beta-lactam, trimethoprim, and quinolone plasmid-mediated resistance genes, which are frequently detected in various media and different treatment processes, have been reported to have significant correlations with intl1. Considering the risk of ARGs, especially those associated with intl1, the removal of intl1 and associated ARGs from water, sludge and livestock manure has attracted much more attention recently. Therefore, the mechanism and removal of intl1 and associated ARGs in water depth treatment, sludge and livestock manure digestion and composting process are reviewed in this paper. Besides, the limitation of the current study in this field is discussed, and the key points in the future investigation are provided.

Keywords

Intl1 Antibiotics resistant gene Water Sludge Livestock manure Treatment 

Notes

Acknowledgements

This work was supported by the National Science Foundation of China (Grant Nos. 51425802 and 51778454), and the Program of Shanghai Subject Chief Scientist (Grant No. 15XD1503400).

References

  1. Aarestrup FM, Agerso Y, Gernersmidt P, Madsen M, Jensen LB (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn Microbiol Infect Dis 37:127–137CrossRefGoogle Scholar
  2. Agga GE, Arthur TM, Durso LM, Harhay DM, Schmidt JW (2015) Antimicrobial-resistant bacterial populations and antimicrobial resistance genes obtained from environments impacted by livestock and municipal waste. PLoS ONE 10:e0132586CrossRefGoogle Scholar
  3. Alekshun MN, Levy SB (1997) Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob Agents Chemother 41:2067Google Scholar
  4. Alexander J, Karaolia P, Fatta-Kassinos D, Schwartz T (2015) Impacts of advanced oxidation processes on microbiomes during wastewater treatment. J Crop Weed 60:127–137Google Scholar
  5. Aminov RI, Garriguesjeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32CrossRefGoogle Scholar
  6. Anderson JC, Carlson JC, Low JE, Challis JK, Wong CS, Knapp CW, Hanson ML (2013) Performance of a constructed wetland in Grand Marais, Manitoba, Canada: Removal of nutrients, pharmaceuticals, and antibiotic resistance genes; from municipal wastewater. Chem Cent J 7:54CrossRefGoogle Scholar
  7. Anderson JC et al (2015) Reducing nutrients, organic micropollutants, antibiotic resistance, and toxicity in rural wastewater effluent with subsurface filtration treatment technology. Ecol Eng 84:375–385CrossRefGoogle Scholar
  8. Andreozzi R, Raffaele M, Nicklas P (2003) Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50:1319–1330CrossRefGoogle Scholar
  9. Angot P, Vergnaud M, Auzou M, Leclercq R (2000) Macrolide Resistance Phenotypes and Genotypes in French Clinical Isolates of Streptococcus pneumoniae. Eur J Clin Microbiol Infect Dis 19:755–758CrossRefGoogle Scholar
  10. Apley MD, Bush EJ, Morrison RB, Singer RS, Snelson H (2012) Use estimates of in-feed antimicrobials in swine production in the United States. Foodborne Pathog Dis 9:272CrossRefGoogle Scholar
  11. Appels L, Houtmeyers S, Degrève J, Van IJ, Dewil R (2013) Influence of microwave pre-treatment on sludge solubilization and pilot scale semi-continuous anaerobic digestion. Biores Technol 128:598–603CrossRefGoogle Scholar
  12. Auerbach EA, Seyfried EE, Mcmahon KD (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res 41:1143–1151CrossRefGoogle Scholar
  13. Aydin S, Ince B, Ince O (2015) Development of antibiotic resistance genes in microbial communities during long-term operation of anaerobic reactors in the treatment of pharmaceutical wastewater. Water Res 83:337CrossRefGoogle Scholar
  14. Baquero F, Martínez JL, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265CrossRefGoogle Scholar
  15. Barraud O, Baclet MC, Denis F, Ploy MC (2010) Quantitative multiplex real-time PCR for detecting class 1, 2 and 3 integrons. J Antimicrob Chemother 65:1642CrossRefGoogle Scholar
  16. Barraud O, Casellas M, Dagot C, Ploy MC (2013) An antibiotic-resistant class 3 integron in an Enterobacter cloacae isolate from hospital effluent. Clin Microbiol Infect 19:E306–E308CrossRefGoogle Scholar
  17. Bennett PM (2008) Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153(Suppl 1):S347Google Scholar
  18. Berendonk TU et al (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13:310CrossRefGoogle Scholar
  19. Blair JM, Al E (2015) Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13:42CrossRefGoogle Scholar
  20. Bohrerova Z, Rosenblum J, Linden KG (2014) Importance of recovery of E. coli in water following ultraviolet light disinfection. J Environ Eng 141:04014094CrossRefGoogle Scholar
  21. Breazeal MVR, Novak JT, Vikesland PJ, Pruden A (2013) Effect of wastewater colloids on membrane removal of antibiotic resistance genes. Water Res 47:130–140CrossRefGoogle Scholar
  22. Burch TR, Sadowsky MJ, Lapara TM (2014) Fate of antibiotic resistance genes and class 1 integrons in soil microcosms following the application of treated residual municipal wastewater solids. Environ Sci Technol 48:5620–5627CrossRefGoogle Scholar
  23. Cano R, Nielfa A, Fdz-Polanco M (2014) Thermal hydrolysis integration in the anaerobic digestion process of different solid wastes: energy and economic feasibility study. Biores Technol 168:14–22CrossRefGoogle Scholar
  24. Cardinal P et al (2014) Macrophytes may not contribute significantly to removal of nutrients, pharmaceuticals, and antibiotic resistance in model surface constructed wetlands. Sci Total Environ 482–483:294CrossRefGoogle Scholar
  25. Cesare AD, Fontaneto D, Doppelbauer J, Corno G (2016) Fitness and recovery of bacterial communities and antibiotic resistance genes in urban wastewaters exposed to classical disinfection treatments. Environ Sci Technol 50:10153–10161CrossRefGoogle Scholar
  26. Chang PH, Juhrend B, Olson TM, Marrs CF, Wigginton KR (2017) Degradation of extracellular antibiotic resistance genes with UV254 treatment. Environ Sci Technol 51:6185–6192CrossRefGoogle Scholar
  27. 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 47:8157–8163Google Scholar
  28. Chen J, Yu Z, Michel F, Wittum T, 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 73:4407CrossRefGoogle Scholar
  29. Chen J et al (2015) Removal of antibiotics and antibiotic resistance genes in rural wastewater by an integrated constructed wetland. Environ Sci Pollut Res Int 22:1794CrossRefGoogle Scholar
  30. Cheng H, Hong PY (2017) Removal of antibiotic-resistant bacteria and antibiotic resistance genes affected by varying degrees of fouling on anaerobic microfiltration membranes. Environ Sci Technol 51:12200CrossRefGoogle Scholar
  31. Chung CT, Niemela SL, Miller RH (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci USA 86:2172CrossRefGoogle Scholar
  32. Cipparone LA, Diehl AC, Speitel GE (1997) Ozonation and BDOC removal: effect on water quality. J Am Water Works Assoc 89:84–97CrossRefGoogle Scholar
  33. Colom K, Pérez J, Alonso R, Fernández-Aranguiz A, Lariño E, Cisterna R (2010) Simple and reliable multiplex PCR assay for detection of bla TEM, bla SHV and bla OXA-1 genes in Enterobacteriaceae. FEMS Microbiol Lett 223:147–151CrossRefGoogle Scholar
  34. Conza JAD, Gutkind GO (2010) Integrones: los coleccionistas de genes Integrons: gene collectors. Rev Argent Microbiol 42:63–78Google Scholar
  35. Cui E, Ying W, Zuo Y, Hong C (2016) Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Biores Technol 203:11CrossRefGoogle Scholar
  36. Cutler TD, Zimmerman JJ (2011) Ultraviolet irradiation and the mechanisms underlying its inactivation of infectious agents. Anim Health Res Rev 12:15–23CrossRefGoogle Scholar
  37. Czekalski N, Gascón DE, Bürgmann H (2014) Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME J 8:1381CrossRefGoogle Scholar
  38. Dahmen S, Mansour W, Boujaafar N, Arlet G, Bouallègue O (2010) Distribution of cotrimoxazole resistance genes associated with class 1 integrons in clinical isolates of Enterobacteriaceae in a university hospital in Tunisia. Microb Drug Resist 16:43CrossRefGoogle Scholar
  39. Di CJ, Gutkind GO (2010) Integrons: gene collectors. Rev Argent Microbiol 42:63–78Google Scholar
  40. Diehl DL, Lapara TM (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 44:9128–9133CrossRefGoogle Scholar
  41. Dobosz S, Goryczko K, Żakowski Ł, Ciereszko A (2005) Effects of UV irradiation and hydrogen peroxide on DNA fragmentation, motility and fertilizing ability of rainbow trout (Oncorhynchus mykiss) spermatozoa. Theriogenology 64:1809–1822CrossRefGoogle Scholar
  42. Dodd MC (2012) Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J Environ Monit 14:1754CrossRefGoogle Scholar
  43. Du J, Geng J, Ren H, Ding L, Xu K, Zhang Y (2015) Variation of antibiotic resistance genes in municipal wastewater treatment plant with A(2)O-MBR system. Environ Sci Pollut Res 22:3715CrossRefGoogle Scholar
  44. Fang H et al (2017) Occurrence and elimination of antibiotic resistance genes in a long-term operation integrated surface flow constructed wetland. Chemosphere 173:99–106CrossRefGoogle Scholar
  45. Fiorentino A, Ferro G, Alferez MC, Pololópez MI, Fernándezibañez P, Rizzo L (2015) Inactivation and regrowth of multidrug resistant bacteria in urban wastewater after disinfection by solar-driven and chlorination processes. J Photochem Photobiol B 148:43CrossRefGoogle Scholar
  46. Gao B, Liu B, Chen T, Yue Q (2011a) Effect of aging period on the characteristics and coagulation behavior of polyferric chloride and polyferric chloride–polyamine composite coagulant for synthetic dying wastewater treatment. J Hazard Mater 187:413–420CrossRefGoogle Scholar
  47. Gao WJ, Lin HJ, Leung KT, Schraft H, Liao BQ (2011b) Structure of cake layer in a submerged anaerobic membrane bioreactor. J Membr Sci 374:110–120CrossRefGoogle Scholar
  48. Gao P, Munir M, Xagoraraki I (2012) Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 421–422:173–183CrossRefGoogle Scholar
  49. Gaveau A, Coetsier C, Roques C, Bacchin P, Dague E, Causserand C (2017) Bacteria transfer by deformation through microfiltration membrane. J Membr Sci 523:446–455CrossRefGoogle Scholar
  50. Gaze WH et al (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5:1253CrossRefGoogle Scholar
  51. Ghosh S, Ramsden SJ, Lapara TM (2009) 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 84:791–796CrossRefGoogle Scholar
  52. Gootz TD (2010) The global problem of antibiotic resistance. Crit Rev Immunol 30:79–93CrossRefGoogle Scholar
  53. Görner H (1994) Photochemistry of DNA and related biomolecules: quantum yields and consequences of photoionization. J Photochem Photobiol B 26:117–139CrossRefGoogle Scholar
  54. Guo MT, Yuan QB, Yang J (2015) Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environ Sci Technol 49:5771–5778CrossRefGoogle Scholar
  55. Hall RM, Collis CM (1995) Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol Microbiol 15:593CrossRefGoogle Scholar
  56. Hall J, Brockhurst MA, Harrison E (2017) Sampling the mobile gene pool: innovation via horizontal gene transfer in bacteria. Philos Trans R Soc B Biol Sci 372:20160424CrossRefGoogle Scholar
  57. He Y, Li L, Zong MH, Alam MJ, Shinoda S, Shi L (2010) Occurrence and characteristics of class 1 and 2 integrons in clinical bacterial isolates from patients in South China. J Health Sci 56:442–450CrossRefGoogle Scholar
  58. He LY et al (2014) Dissemination of antibiotic resistance genes in representative broiler feedlots environments: identification of indicator ARGs and correlations with environmental variables. Environ Sci Technol 48:13120CrossRefGoogle Scholar
  59. Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5CrossRefGoogle Scholar
  60. Helling A et al (2016) Passage of soft pathogens through microfiltration membranes scales with transmembrane pressure. J Membr Sci 522:292–302CrossRefGoogle Scholar
  61. Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236CrossRefGoogle Scholar
  62. Hoek EM, Elimelech M (2003) Cake-enhanced concentration polarization: a new fouling mechanism for salt-rejecting membranes. Environ Sci Technol 37:5581–5588CrossRefGoogle Scholar
  63. Hong SM, Park JK, Lee YO (2004) Mechanisms of microwave irradiation involved in the destruction of fecal coliforms from biosolids. Water Res 38:1615–1625CrossRefGoogle Scholar
  64. Hua F, Wang H, Lin C, Yu Y (2015) Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environ Sci Technol 49:1095CrossRefGoogle Scholar
  65. Huang X, Liu C, Wang Z, Gao C, Zhu G, Liu L (2013) The effects of different substrates on ammonium removal in constructed wetlands: a comparison of their physicochemical characteristics and ammonium-oxidizing prokaryotic communities. Clean Soil Air Water 41:283–290CrossRefGoogle Scholar
  66. Huang X, Liu C, Li K, Su J, Zhu G, Liu L (2015) Performance of vertical up-flow constructed wetlands on swine wastewater containing tetracyclines and TET genes. Water Res 70:109–117CrossRefGoogle Scholar
  67. Huang H, Chen Y, Zheng X, Su Y, Wan R, Yang S (2016) Distribution of tetracycline resistance genes in anaerobic treatment of waste sludge: The role of pH in regulating tetracycline resistant bacteria and horizontal gene transfer. Biores Technol 218:1284–1289CrossRefGoogle Scholar
  68. Huang H, Zheng X, Chen Y, Liu H, Wan R, Su Y (2017a) Alkaline fermentation of waste sludge causes a significant reduction of antibiotic resistance genes in anaerobic reactors. Sci Total Environ 580:380–387CrossRefGoogle Scholar
  69. Huang X, Zheng J, Liu C, Liu L, Liu Y, Fan H (2017b) Removal of antibiotics and resistance genes from swine wastewater using vertical flow constructed wetlands: effect of hydraulic flow direction and substrate type. Chem Eng J 308:692–699CrossRefGoogle Scholar
  70. Imai A, Fukushima T, Matsushige K, Kim YH, Choi K (2002) Characterization of dissolved organic matter in effluents from wastewater treatment plants. Water Res 36:859–870CrossRefGoogle Scholar
  71. Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 96:3801–3806CrossRefGoogle Scholar
  72. Janssen EM, Erickson PR, Mcneill K (2014) Dual roles of dissolved organic matter as sensitizer and quencher in the photooxidation of tryptophan. Environ Sci Technol 48:4916–4924CrossRefGoogle Scholar
  73. Jeon B, Wang Y, Hao H, Barton YW, Zhang Q (2011) Contribution of CmeG to antibiotic and oxidative stress resistance in Campylobacter jejuni. J Antimicrob Chemother 66:79–85CrossRefGoogle Scholar
  74. Jiménez J, Guardia-Puebla Y, Cisneros-Ortiz ME, Morgan-Sagastume JM, Guerra G, Noyola A (2015) Optimization of the specific methanogenic activity during the anaerobic co-digestion of pig manure and rice straw, using industrial clay residues as inorganic additive. Chem Eng J 259:703–714CrossRefGoogle Scholar
  75. Joy SR, Li X, Snow DD, Gilley JE, Woodbury B, Bartelthunt SL (2014) Fate of antimicrobials and antimicrobial resistance genes in simulated swine manure storage. Sci Total Environ 481:69–74CrossRefGoogle Scholar
  76. Kay E, Vogel TM, Bertolla F, Nalin R, Simonet P (2002) In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl Environ Microbiol 68:3345–3351CrossRefGoogle Scholar
  77. Khan GA, Berglund B, Khan KM, Lindgren PE, Fick J (2013) Occurrence and abundance of antibiotics and resistance genes in rivers, canal and near drug formulation facilities—a study in Pakistan. PLoS ONE 8:e62712CrossRefGoogle Scholar
  78. Kim YB, Jeon JH, Choi S, Shin J, Lee Y, Kim YM (2018) Use of a filtering process to remove solid waste and antibiotic resistance genes from effluent of a flow-through fish farm. Sci Total Environ 615:289–296CrossRefGoogle Scholar
  79. Koike S, Aminov RI, Yannarell AC, Gans HD, Krapac IG, Cheesanford JC, Mackie RI (2010) Molecular ecology of macrolide–lincosamide–streptogramin B methylases in waste lagoons and subsurface waters associated with swine production. Microb Ecol 59:487–498CrossRefGoogle Scholar
  80. Koonin EV, Makarova KS, Aravind L (2003) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742CrossRefGoogle Scholar
  81. Kuglarz M, Karakashev D, Angelidaki I (2013) Microwave and thermal pretreatment as methods for increasing the biogas potential of secondary sludge from municipal wastewater treatment plants. Biores Technol 134:290CrossRefGoogle Scholar
  82. Lapara TM, Burch TR, Mcnamara PJ, Tan DT, Yan M, Eichmiller JJ (2011) Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into duluth-superior harbor. Environ Sci Technol 45:9543CrossRefGoogle Scholar
  83. Lavilla S et al (2008) Prevalence of QNR genes among extended-spectrum beta-lactamase-producing enterobacterial isolates in Barcelona, Spain. J Antimicrob Chemother 61:291CrossRefGoogle Scholar
  84. Le TH et al (2016) Occurrences and characterization of antibiotic-resistant bacteria and genetic determinants of hospital wastewater in a tropical country. Antimicrob Agents Chemother 60:7449CrossRefGoogle Scholar
  85. Lee M, Hidaka T, Hagiwara W, Tsuno H (2009) Comparative performance and microbial diversity of hyperthermophilic and thermophilic co-digestion of kitchen garbage and excess sludge. Biores Technol 100:578–585CrossRefGoogle Scholar
  86. Lei GY, Ma J, Guan XH, Song AK, Cui YJ (2009) Effect of basicity on coagulation performance of polyferric chloride applied in eutrophicated raw water. Desalination 247:518–529CrossRefGoogle Scholar
  87. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:S122CrossRefGoogle Scholar
  88. Li N, Sheng GP, Lu YZ, Zeng RJ, Yu HQ (2017) Removal of antibiotic resistance genes from wastewater treatment plant effluent by coagulation. Water Res 111:204–212CrossRefGoogle Scholar
  89. Liu X, Liu L, Wang Y, Wang X, Ma Y, Li Y (2014) The Study on the factors affecting transformation efficiency of E. coli competent cells. Pak J Pharm Sci 27:679Google Scholar
  90. Liu J, Tong J, Wei Y, Wang Y (2015) Microwave and its combined processes: An effective way for enhancing anaerobic digestion and dewaterability of sewage sludge? Journal of Water Reuse & Desalination 5:264CrossRefGoogle Scholar
  91. Liu J, Jia R, Wang Y, Wei Y, Zhang J, Rui W, Xing C (2017) Does residual H2O2 result in inhibitory effect on enhanced anaerobic digestion of sludge pretreated by microwave-H2O2 pretreatment process? Environ Sci Pollut Res 24:9016CrossRefGoogle Scholar
  92. Llorens E, Matamoros V, Domingo V, Bayona JM, García J (2009) Water quality improvement in a full-scale tertiary constructed wetland: effects on conventional and specific organic contaminants. Sci Total Environ 407:2517–2524CrossRefGoogle Scholar
  93. Luo J, Feng L, Chen Y, Sun H, Shen Q, Li X, Chen H (2015) Alkyl polyglucose enhancing propionic acid enriched short-chain fatty acids production during anaerobic treatment of waste activated sludge and mechanisms. Water Res 73:332–341CrossRefGoogle Scholar
  94. Ma Y, Wilson CA, Novak JT, Riffat R, Aynur S, Murthy S, Pruden A (2011) Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environ Sci Technol 45:7855CrossRefGoogle Scholar
  95. Maal-Bared R, Bartlett KH, Bowie WR, Hall ER (2013) Phenotypic antibiotic resistance of Escherichia coli and E. coli O157 isolated from water, sediment and biofilms in an agricultural watershed in British Columbia. Sci Total Environ 443:315CrossRefGoogle Scholar
  96. Makowska N, Koczura R, Mokracka J (2016) Class 1 integrase, sulfonamide and tetracycline resistance genes in wastewater treatment plant and surface water. Chemosphere 144:1665–1673CrossRefGoogle Scholar
  97. Marchand L, Mench M, Jacob DL, Otte ML (2010) Metal and metalloid removal in constructed wetlands, with emphasis on the importance of plants and standardized measurements: a review. Environ Pollut 158:3447–3461CrossRefGoogle Scholar
  98. Marti E, Monclús H, Jofre J, Rodriguez-Roda I, Comas J, Balcázar JL (2011) Removal of microbial indicators from municipal wastewater by a membrane bioreactor (MBR). Biores Technol 102:5004–5009CrossRefGoogle Scholar
  99. Marti E, Jofre J, Balcazar JL (2013) Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS ONE 8:e78906CrossRefGoogle Scholar
  100. Martínez JL, Coque TM, Baquero F (2015) What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13:116CrossRefGoogle Scholar
  101. Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608CrossRefGoogle Scholar
  102. McKinney CW, Pruden A (2012) Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ Sci Technol 46:13393–13400CrossRefGoogle Scholar
  103. Miller JH, Novak JT, Knocke WR, Pruden A (2015) Elevation of antibiotic resistance genes at cold temperatures: implications for winter storage of sludge and biosolids. Lett Appl Microbiol 59:587–593CrossRefGoogle Scholar
  104. Monier JM, Demanèche S, Delmont TO, Mathieu A, Vogel TM, Simonet P (2011) Metagenomic exploration of antibiotic resistance in soil. Curr Opin Microbiol 14:229CrossRefGoogle Scholar
  105. Moreira NFF et al (2016) Photocatalytic ozonation of urban wastewater and surface water using immobilized TiO2 with LEDs: Micropollutants, antibiotic resistance genes and estrogenic activity. Water Res 94:10–22CrossRefGoogle Scholar
  106. Mu Q, Li J, Sun Y, Mao D, Wang Q, Luo Y (2015) Occurrence of sulfonamide-, tetracycline-, plasmid-mediated quinolone- and macrolide-resistance genes in livestock feedlots in Northern China. Environ Sci Pollut Res Int 22:6932CrossRefGoogle Scholar
  107. Munck C, Albertsen M, Telke A, Ellabaan M, Nielsen PH, Sommer MOA (2015) Limited dissemination of the wastewater treatment plant core resistome. Nat Commun 6:CD003849CrossRefGoogle Scholar
  108. 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 45:681–693CrossRefGoogle Scholar
  109. Navaee-Ardeh S, Bertrand F, Stuart PR (2010) Key variables analysis of a novel continuous biodrying process for drying mixed sludge. Biores Technol 101:3379–3387CrossRefGoogle Scholar
  110. Ndi OL, Barton MD (2011) Incidence of class 1 integron and other antibiotic resistance determinants in Aeromonas spp. from rainbow trout farms in Australia. J Fish Dis 34:589–599CrossRefGoogle Scholar
  111. Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209CrossRefGoogle Scholar
  112. Nõlvak H et al (2013) Dynamics of antibiotic resistance genes and their relationships with system treatment efficiency in a horizontal subsurface flow constructed wetland. Sci Total Environ 461–462:636CrossRefGoogle Scholar
  113. Novak JT, Sadler ME, Murthy SN (2003) Mechanisms of floc destruction during anaerobic and aerobic digestion and the effect on conditioning and dewatering of biosolids. Water Res 37:3136–3144CrossRefGoogle Scholar
  114. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299CrossRefGoogle Scholar
  115. Partridge SR, Tsafnat G, Coiera E, Iredell JR (2009) Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33:757CrossRefGoogle Scholar
  116. Partridge SR, Tsafnat G, Coiera E, Iredell JR (2010) Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33:757–784CrossRefGoogle Scholar
  117. Pasmore M, Todd P, Smith S, Baker D, Silverstein JA, Coons D, Bowman CN (2001) Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling. J Membr Sci 194:15–32CrossRefGoogle Scholar
  118. Pei R, Kim SC, Carlson KH, Pruden A (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40:2427–2435CrossRefGoogle Scholar
  119. Qian X, Sun W, Gu J, Wang XJ, Sun JJ, Yin YN, Duan ML (2016a) Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. J Hazard Mater 315:61CrossRefGoogle Scholar
  120. Qian X et al (2016b) Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresour Technol 220:425–432CrossRefGoogle Scholar
  121. Recchia GD, Hall RM (1995) Gene cassettes: a new class of mobile element. Microbiology 141(Pt 12):3015CrossRefGoogle Scholar
  122. Rizzo L et al (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360CrossRefGoogle Scholar
  123. Rodriguezmozaz S, Chamorro S, Marti E, Huerta B, Gros M, Borrego CM (2015) Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res 69:234–242CrossRefGoogle Scholar
  124. 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 31:449CrossRefGoogle Scholar
  125. Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51:267–276CrossRefGoogle Scholar
  126. Selvam A, Xu D, Zhao Z, Wong JWC (2012a) Fate of tetracycline, sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure. Biores Technol 126:383CrossRefGoogle Scholar
  127. Selvam A, Zhao Z, Wong JWC (2012b) Composting of swine manure spiked with sulfadiazine, chlortetracycline and ciprofloxacin. Biores Technol 126:412–417CrossRefGoogle Scholar
  128. Shah SQ, Colquhoun DJ, Nikuli HL, Sørum H (2012) Prevalence of antibiotic resistance genes in the bacterial flora of integrated fish farming environments of Pakistan and Tanzania. Environ Sci Technol 46:8672–8679CrossRefGoogle Scholar
  129. Shi JG, Zeng GM, Yuan XZ, Dai F, Liu J, Wu XH (2006) The stimulatory effects of surfactants on composting of waste rich in cellulose. World J Microbiol Biotechnol 22:1121–1127CrossRefGoogle Scholar
  130. Singer AC, Shaw H, Rhodes V, Hart A (2016) Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front Microbiol 7:1728CrossRefGoogle Scholar
  131. Sköld O (2000) Sulfonamide resistance: mechanisms and trends. Drug Resist Updates 3:155–160CrossRefGoogle Scholar
  132. Smith MS et al (2004) Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 70:7372–7377CrossRefGoogle Scholar
  133. Snyder L, Champness W, Snyder L, Champness W (2010) Molecular genetics of bacteria. Q Rev Biol 71:1237Google Scholar
  134. Song W et al (2017) Effects of different swine manure to wheat straw ratios on antibiotic resistance genes and the microbial community structure during anaerobic digestion. Biores Technol 231:1–8CrossRefGoogle Scholar
  135. Sousa JM et al (2016) Ozonation and UV 254 nm radiation for the removal of microorganisms and antibiotic resistance genes from urban wastewater. J Hazard Mater 323:434–441CrossRefGoogle Scholar
  136. Stalder T, Barraud O, Jové T, Casellas M, Gaschet M, Dagot C, Ploy MC (2014) Quantitative and qualitative impact of hospital effluent on dissemination of the integron pool. ISME J 8:768–777CrossRefGoogle Scholar
  137. Stecher B, Maier L, Hardt WD (2013) ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11:277CrossRefGoogle Scholar
  138. Stokes HW, Hall RM (2010) A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3:1669–1683CrossRefGoogle Scholar
  139. Stokes HW, Nesbø CL, Holley M, Bahl MI, Gillings MR, Yan B (2006) Class 1 integrons potentially predating the association with Tn402-like transposition genes are present in a sediment microbial community. Packag Eng 188:5722Google Scholar
  140. Su HC, Ying GG, Ran T, Zhang RQ, Zhao JL, Liu YS (2012) Class 1 and 2 integrons, sul resistance genes and antibiotic resistance in Escherichia coli isolated from Dongjiang River, South China. Environ Pollut 169:42–49CrossRefGoogle Scholar
  141. Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363CrossRefGoogle Scholar
  142. Sui Q, Zhang J, Chen M, Tong J, Wang R, Wei Y (2016) Distribution of antibiotic resistance genes (ARGs) in anaerobic digestion and land application of swine wastewater. Environ Pollut 213:751CrossRefGoogle Scholar
  143. Sun W, Qian X, Gu J, Wang XJ, Zhang L, Guo AY (2017) Mechanisms and effects of arsanilic acid on antibiotic resistance genes and microbial communities during pig manure digestion. Bioresour Technol 234:217–223CrossRefGoogle Scholar
  144. Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L (1996) Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40:2562–2566Google Scholar
  145. Thayanukul P, Kurisu F, Kasuga I, Furumai H (2013) Evaluation of microbial regrowth potential by assimilable organic carbon in various reclaimed water and distribution systems. Water Res 47:225–232CrossRefGoogle Scholar
  146. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721CrossRefGoogle Scholar
  147. Tian Z, Zhang Y, Yu B, Yang M (2016) Changes of resistome, mobilome and potential hosts of antibiotic resistance genes during the transformation of anaerobic digestion from mesophilic to thermophilic. Water Res 98:261CrossRefGoogle Scholar
  148. Tong J, Liu J, Zheng X, Zhang J, Ni X, Chen M, Wei Y (2016) Fate of antibiotic resistance bacteria and genes during enhanced anaerobic digestion of sewage sludge by microwave pretreatment. Biores Technol 217:37–43CrossRefGoogle Scholar
  149. Turker G, Akyol Ç, Ince O, Aydin S, Ince B (2017) Operating conditions influence microbial community structures, elimination of the antibiotic resistance genes and metabolites during anaerobic digestion of cow manure in the presence of oxytetracycline. Ecotoxicol Environ Saf 147:349CrossRefGoogle Scholar
  150. Vacca G, Wand H, Nikolausz M, Kuschk P, Kästner M (2005) Effect of plants and filter materials on bacteria removal in pilot-scale constructed wetlands. Water Res 39:1361–1373CrossRefGoogle Scholar
  151. Verhoeven JTA, Meuleman AFM (1999) Wetlands for wastewater treatment: opportunities and limitations. Ecol Eng 12:5–12CrossRefGoogle Scholar
  152. Versporten A et al (2014) Antibiotic use in eastern Europe: a cross-national database study in coordination with the WHO Regional Office for Europe. Lancet Infect Dis 14:381–387CrossRefGoogle Scholar
  153. Volokhov D, Chizhikov V, Chumakov K, Rasooly A (2010) Microarray analysis of erythromycin resistance determinants. J Appl Microbiol 95:787–798CrossRefGoogle Scholar
  154. Vrijenhoek EM, Hong S, Elimelech M (2001) Influence of membrane surface properties on initial rate of colloidal fouling of reverse osmosis and nanofiltration membranes. J Membr Sci 188:115–128CrossRefGoogle Scholar
  155. Vymazal J (2007) Removal of nutrients in various types of constructed wetlands. Sci Total Environ 380:48–65CrossRefGoogle Scholar
  156. Wang Y, Wei Y, Liu J (2009) Effect of H2O2 dosing strategy on sludge pretreatment by microwave-H2O2 advanced oxidation process. J Hazard Mater 169:680CrossRefGoogle Scholar
  157. Ward AJ, Hobbs PJ, Holliman PJ, Jones DL (2008) Optimisation of the anaerobic digestion of agricultural resources. Biores Technol 99:7928–7940CrossRefGoogle Scholar
  158. Wei YS, Fan YB, Wang MJ, Wang JS (2000) Composting and compost application in China. Resour Conserv Recycl 30:277–300CrossRefGoogle Scholar
  159. Wiedenbeck J, Cohan FM (2011) Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35:957–976CrossRefGoogle Scholar
  160. Wilcks A, van Hoek AH, Joosten RG, Jacobsen BB, Aarts HJ (2004) Persistence of DNA studied in different ex vivo and in vivo rat models simulating the human gut situation. Food Chem Toxicol 42:493–502CrossRefGoogle Scholar
  161. Willems RJ, Hanage WP, Bessen DE, Feil EJ (2011) Population biology of Gram-positive pathogens: high-risk clones for dissemination of antibiotic resistance. FEMS Microbiol Rev 35:872–900CrossRefGoogle Scholar
  162. Williams MC, Wenner JR, Rouzina I, Bloomfield VA (2001) Effect of pH on the overstretching transition of double-stranded DNA: evidence of force-induced DNA melting. Biophys J 80:874–881CrossRefGoogle Scholar
  163. Winkler MK, Bennenbroek MH, Horstink FH, van Loosdrecht MC, Gj VDP (2013) The biodrying concept: an innovative technology creating energy from sewage sludge. Biores Technol 147:124–129CrossRefGoogle Scholar
  164. Wu J, Le-Clech P, Stuetz RM, Fane AG, Chen V (2008) Effects of relaxation and backwashing conditions on fouling in membrane bioreactor. J Membr Sci 324:26–32CrossRefGoogle Scholar
  165. Wu N, Qiao M, Zhang B, Cheng WD, Zhu YG (2010) Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ Sci Technol 44:6933–6939CrossRefGoogle Scholar
  166. Wu Y, Cui E, Zuo Y, Cheng W, Rensing C, Chen H (2016) Influence of two-phase anaerobic digestion on fate of selected antibiotic resistance genes and class I integrons in municipal wastewater sludge. Biores Technol 211:414CrossRefGoogle Scholar
  167. Xi B, Liu H, Huang GH, Zhang B, Qin X (2005) Effect of bio-surfactant on municipal solid waste composting process. J Environ Sci 17:409–413Google Scholar
  168. Xiao F, Simcik MF, Gulliver JS (2013) Mechanisms for removal of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) from drinking water by conventional and enhanced coagulation. Water Res 47:49–56CrossRefGoogle Scholar
  169. Xiong J, Fu D, Singh RP, Ducoste JJ (2016a) Structural characteristics and development of the cake layer in a dynamic membrane bioreactor. Sep Purif Technol 167:88–96CrossRefGoogle Scholar
  170. Xiong Y, Harb M, Hong PY (2016b) Characterization of biofoulants illustrates different membrane fouling mechanisms for aerobic and anaerobic membrane bioreactors. Sep Purif Technol 157:192–202CrossRefGoogle Scholar
  171. Yang X, Shang C, Huang JC (2005) DBP formation in breakpoint chlorination of wastewater. Water Res 39:4755–4767CrossRefGoogle Scholar
  172. Yang Y et al (2012) Quantification and characterization of β-lactam resistance genes in 15 sewage treatment plants from East Asia and North America. Appl Microbiol Biotechnol 95:1351CrossRefGoogle Scholar
  173. Yang Y, Li B, Zou S, Fang HH, Zhang T (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res 62:97CrossRefGoogle Scholar
  174. Yi L, Mao DQ, Rysz M, Zhou QX, Zhang HJ, Lin X, Alvarez PJJ (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44:7220CrossRefGoogle Scholar
  175. Yin Y et al (2017) Effects of copper addition on copper resistance, antibiotic resistance genes, and intl1 during swine manure composting. Front Microbiol 8:344Google Scholar
  176. Zeng T, Wilson CJ, Mitch WA (2014) Effect of chemical oxidation on the sorption tendency of dissolved organic matter to a model hydrophobic surface. Environ Sci Technol 48:5118CrossRefGoogle Scholar
  177. Zhang XX et al (2009) Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology 18:652CrossRefGoogle Scholar
  178. Zhang J et al (2015a) Effects of aeration strategy on the evolution of dissolved organic matter (DOM) and microbial community structure during sludge bio-drying. Appl Microbiol Biotechnol 99:7321CrossRefGoogle Scholar
  179. Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015b) Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Technol 49:6772CrossRefGoogle Scholar
  180. Zhang T, Mao C, Zhai N, Wang X, Yang G (2015c) Influence of initial pH on thermophilic anaerobic co-digestion of swine manure and maize stalk. Waste Manag 35:119–126CrossRefGoogle Scholar
  181. Zhang T, Yang Y, Pruden A (2015d) Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Appl Microbiol Biotechnol 99:7771CrossRefGoogle Scholar
  182. Zhang J et al (2016a) Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting. Water Res 91:339–349CrossRefGoogle Scholar
  183. Zhang J, Chen M, Sui Q, Wang R, Tong J, Wei Y (2016b) Fate of antibiotic resistance genes and its drivers during anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment. Biores Technol 217:28CrossRefGoogle Scholar
  184. Zhang J, Sui Q, Tong J, Buhe C, Wang R, Chen M, Wei Y (2016c) Sludge bio-drying: Effective to reduce both antibiotic resistance genes and mobile genetic elements. Water Res 106:62–70CrossRefGoogle Scholar
  185. Zhang R et al (2016d) Relationships between sulfachloropyridazine sodium, zinc, and sulfonamide resistance genes during the anaerobic digestion of swine manure. Biores Technol 225:343CrossRefGoogle Scholar
  186. Zhang Y et al (2016e) Effects of adding different surfactants on antibiotic resistance genes and intI1 during chicken manure composting. Biores Technol 219:545CrossRefGoogle Scholar
  187. Zhang J et al (2017) Profiles and drivers of antibiotic resistance genes distribution in one-stage and two-stage sludge anaerobic digestion based on microwave-H2O2 pretreatment. Biores Technol 241:573CrossRefGoogle Scholar
  188. Zhao L, Dong YH, Wang H (2010a) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075CrossRefGoogle Scholar
  189. Zhao L, Gu WM, He PJ, Shao LM (2010b) Effect of air-flow rate and turning frequency on bio-drying of dewatered sludge. Water Res 44:6144CrossRefGoogle Scholar
  190. Zhao L, Gu WM, He PJ, Shao LM (2011) Biodegradation potential of bulking agents used in sludge bio-drying and their contribution to bio-generated heat. Water Res 45:2322–2330CrossRefGoogle Scholar
  191. Zhao X, Hu HY, Yu T, Su C, Jiang H, Liu S (2014) Effect of different molecular weight organic components on the increase of microbial growth potential of secondary effluent by ozonation. J Environ Sci 26:2190–2197CrossRefGoogle Scholar
  192. Zheng J, Su C, Zhou J, Xu L, Qian Y, Chen H (2017) Effects and mechanisms of ultraviolet, chlorination, and ozone disinfection on antibiotic resistance genes in secondary effluents of municipal wastewater treatment plants. Chem Eng J 317:309–316CrossRefGoogle Scholar
  193. Zhu YG et al (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110:3435CrossRefGoogle Scholar
  194. Zhuang Y, Ren H, Geng J, Zhang Y, Zhang Y, Ding L, Xu K (2015) Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environ Sci Pollut Res 22:7037CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Pollution Control and Resource Reuse, School of Environmental Science and EngineeringTongji UniversityShanghaiChina

Personalised recommendations