Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater

Water Research

Volumn 95, Issue , 2016, Pages 11-18

  Calero Cáceres, William ^a   Muniesa, Maite ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Antibiotic resistance; Bacteriophages; Public health; Wastewater

Indexed keywords

ANTIBIOTICS; BINARY ALLOYS; ESCHERICHIA COLI; GENES; POLYMERASE CHAIN REACTION; WASTEWATER TREATMENT;

ANTIBIOTIC RESISTANCE GENES; ANTIBIOTICS RESISTANCE; C VALUES; GENETIC ELEMENTS; GLOBAL HEALTH; HEALTH CONCERNS; NATURALLY OCCURRING; PH VALUE; RAW WASTEWATERS; WATERBODIES;

BACTERIOPHAGES;

BACTERIOPHAGE DNA; BETA LACTAMASE CTX M; BETA LACTAMASE TEM 1; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; BACTERIOPHAGE; CHLORINATION; COLIFORM BACTERIUM; DISINFECTION; EMERGENCE; GENETIC ANALYSIS; MESOCOSM; PERSISTENCE; PH; PUBLIC HEALTH; TEMPERATURE GRADIENT; WASTEWATER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIOPHAGE; CHLORINATION; COLIPHAGE; DISINFECTION; ESCHERICHIA COLI; FRACTIONATION; LIMIT OF DETECTION; MICROBIOLOGICAL PARAMETERS; NONHUMAN; PH; PRIORITY JOURNAL; TEMPERATURE; ULTRAVIOLET RADIATION; WASTE WATER; WASTE WATER MANAGEMENT; WATER SAMPLING; BACTERIUM; DRUG EFFECT; GENETICS; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIOPHAGES; DRUG RESISTANCE, MICROBIAL; GENES, BACTERIAL; WASTE WATER;

EID: 84960397134     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2016.03.006     Document Type: Article

References (58)

1. Allué-Guardia A., Jofre J., Muniesa M. Stability and infectivity of cytolethal distending toxin type V gene-carrying bacteriophages in a water mesocosm and under different inactivation conditions. Appl. Environ. Microbiol. 2012, 78:5818-5823. 10.1128/AEM.00997-12.
2. Allué-Guardia A., Martínez-Castillo A., Muniesa M. Persistence of infectious Shiga toxin-encoding bacteriophages after disinfection treatments. Appl. Environ. Microbiol. 2014, 80:2142-2149. 10.1128/AEM.04006-13.
3. Anonymous ISO 10705-2: Water Quality. Detection and Enumeration of Bacteriophages -part 2: Enumeration of Somatic Coliphages 2000.
4. Auerbach E.A., Seyfried E.E., McMahon K.D. Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res. 2007, 41:1143-1151. 10.1016/j.watres.2006.11.045.
5. Aw T.G., Howe A., Rose J.B. Metagenomic approaches for direct and cell culture evaluation of the virological quality of wastewater. J. Virol. Methods 2014, 210:15-21. 10.1016/j.jviromet.2014.09.017.
6. Aw T.G., Rose J.B. Detection of pathogens in water: from phylochips to qPCR to pyrosequencing. Curr. Opin. Biotechnol. 2012, 23:422-430. 10.1016/j.copbio.2011.11.016.
7. Boletín Oficial del Estado Real Decreto 1620/2007 de 7 de diciembre, por el que se establece el régimen jurídico de la reutilización de las aguas depuradas. BOE núm 2007, 294(21092):46932-46946.
8. Botes M., De Kwaadsteniet M., Cloete T.E. Application of quantitative PCR for the detection of microorganisms in water. Anal. Bioanal. Chem. 2013, 405:91-108. 10.1007/s00216-012-6399-3.
9. Calero-Cáceres W., Melgarejo A., Colomer-Lluch M., Stoll C., Lucena F., Jofre J., Muniesa M. Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions. Environ. Sci. Technol. 2014, 48:7602-7611. 10.1021/es501851s.
10. Cantalupo P.G., Calgua B., Zhao G., Hundesa A., Wier A.D., Katz J.P., Grabe M., Hendrix R.W., Girones R., Wang D., Pipas J.M. Raw sewage harbors diverse viral populations. MBio 2011, 2:e00180-11. 10.1128/mBio.00180-11.
11. Cantón R. Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin. Microbiol. Infect. 2009, 15(Suppl. 1):20-25. 10.1111/j.1469-0691.2008.02679.x.
12. Colomer-Lluch M., Calero-Cáceres W., Jebri S., Hmaied F., Muniesa M., Jofre J. Antibiotic resistance genes in bacterial and bacteriophage fractions of Tunisian and Spanish wastewaters as markers to compare the antibiotic resistance patterns in each population. Environ. Int. 2014, 73:167-175. 10.1016/j.envint.2014.07.003.
13. Colomer-Lluch M., Jofre J., Muniesa M. Quinolone resistance genes (qnrA and qnrS) in bacteriophage particles from wastewater samples and the effect of inducing agents on packaged antibiotic resistance genes. J. Antimicrob. Chemother. 2014, 69:1265-1274. 10.1093/jac/dkt528.
14. Colomer-Lluch M., Jofre J., Muniesa M. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 2011, 6.
15. Czekalski N., Berthold T., Caucci S., Egli A., Bürgmann H. Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into lake geneva. Switz. Front. Microbiol. 2012, 3:106. 10.3389/fmicb.2012.00106.
16. Davies J.E. Origins, acquisition and dissemination of antibiotic resistance determinants. Ciba Found. Symp. 1997, 207:15-27. discussion 27-35.
17. Davies-Colley R.J., Donnison A.M., Speed D.J., Ross C.M., Nagels J.W. Inactivation of faecal indicator micro-organisms in waste stabilisation ponds: interactions of environmental factors with sunlight. Water Res. 1999, 33:1220-1230. 10.1016/S0043-1354(98)00321-2.
18. Durán A.E., Muniesa M., Mocé-Llivina L., Campos C., Jofre J., Lucena F. Usefulness of different groups of bacteriophages as model micro-organisms for evaluating chlorination. J. Appl. Microbiol. 2003, 95:29-37. 10.1046/j.1365-2672.2003.t01-1-01948.x.
19. Durán A.E., Muniesa M., Méndez X., Valero F., Lucena F., Jofre J. Removal and inactivation of indicator bacteriophages in fresh waters. J. Appl. Microbiol. 2002, 92:338-347.
20. ECDC/EMEA The bacterial challenge: time to react [WWW document]. Eur. Cent. Dis. Prev. Control 2009, http://ecdc.europa.eu/en/publications/Publications/0909_TER_The_Bacterial_Challenge_Time_to_React.pdf.
21. EFSA-ECDC EU Summary Report on Antimicrobial Resistance in Zoonotic and Indicator Bacteria from Humans, Animals and Food in 2013 2015.
22. Evans T.J., Crow M.A., Williamson N.R., Orme W., Thomson N.R., Komitopoulou E., Salmond G.P.C. Characterization of a broad-host-range flagellum-dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 2010, 156:240-247. 10.1099/mic.0.032797-0.
23. Gonzalez J.M., Sherr E.B., Sherr B.F. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 1990, 56:583-589.
24. Guardabassi L., Lo D.M.A., Wong F., Dalsgaard A. The effects of tertiary wastewater treatment on the prevalence of antimicrobial resistant bacteria. Water Res. 2002, 36:1955-1964.
25. Huang J.-J., Hu H.-Y., Lu S.-Q., Li Y., Tang F., Lu Y., Wei B. Monitoring and evaluation of antibiotic-resistant bacteria at a municipal wastewater treatment plant in China. Environ. Int. 2012, 42:31-36. 10.1016/j.envint.2011.03.001.
26. International Organization for Standardization ISO 9308-1:2014-Water Quality - Enumeration of Escherichia coli and Coliform Bacteria - Part 1: Membrane Filtration Method for Waters with Low Bacterial Background Flora 2014.
27. International Organization for Standardization ISO 10705-2:2000-Water quality - detection and enumeration of bacteriophages - Part 2: enumeration of somatic coliphages [WWW Document]. Int. Organ. Stand 2000.
28. Jończyk E., Kłak M., Miedzybrodzki R., Górski a The influence of external factors on bacteriophages-review. Folia Microbiol. (Praha) 2011, 56:191-200. 10.1007/s12223-011-0039-8.
29. Kerby G.P., Gowdy R.A. Purification pH stability and sedimentation properties of the T7 bacteriophage of Escherichia coli. J. Immunol. 1949, 63:93-107.
30. Khan M.A., Satoh H., Katayama H., Kurisu F., Mino T. Bacteriophages isolated from activated sludge processes and their polyvalency. Water Res. 2002, 36:3364-3370.
31. Lachmayr K.L., Kerkhof L.J., Dirienzo A.G., Cavanaugh C.M., Ford T.E. Quantifying nonspecific TEM beta-lactamase (blaTEM) genes in a wastewater stream. Appl. Environ. Microbiol. 2009, 75:203-211. 10.1128/AEM.01254-08.
32. Langlet J., Gaboriaud F., Gantzer C. Effects of pH on plaque forming unit counts and aggregation of MS2 bacteriophage. J. Appl. Microbiol. 2007, 103:1632-1638. 10.1111/j.1365-2672.2007.03396.x.
33. LaPara T.M., Burch T.R., McNamara P.J., Tan D.T., Yan M., Eichmiller J.J. Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior Harbor. Environ. Sci. Technol. 2011, 45:9543-9549. 10.1021/es202775r.
34. Lee H.S., Sobsey M.D. Survival of prototype strains of somatic coliphage families in environmental waters and when exposed to UV low-pressure monochromatic radiation or heat. Water Res. 2011, 45:3723-3734. 10.1016/j.watres.2011.04.024.
35. Li B., Yang Y., Ma L., Ju F., Guo F., Tiedje J.M., Zhang T. Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 2015, 1-13. 10.1038/ismej.2015.59.
36. Lucena F., Duran A.E., Morón a, Calderón E., Campos C., Gantzer C., Skraber S., Jofre J. Reduction of bacterial indicators and bacteriophages infecting faecal bacteria in primary and secondary wastewater treatments. J. Appl. Microbiol. 2004, 97:1069-1076. 10.1111/j.1365-2672.2004.02397.x.
37. Marín I., Goñi P., Lasheras A.M., Ormad M.P. Efficiency of a Spanish wastewater treatment plant for removal potentially pathogens: characterization of bacteria and protozoa along water and sludge treatment lines. Ecol. Eng. 2015, 74:28-32. 10.1016/j.ecoleng.2014.09.027.
38. Marti E., Jofre J., Balcazar J.L. Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS One 2013, 8:e78906. 10.1371/journal.pone.0078906.
39. Marti E., Variatza E., Balcázar J.L. Bacteriophages as a reservoir of extended-spectrum β-lactamase and fluoroquinolone resistance genes in the environment. Clin. Microbiol. Infect. 2014, 20:O456-O459. 10.1111/1469-0691.12446.
40. McKinney C.W., Pruden A. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 2012, 46:13393-13400. 10.1021/es303652q.
41. Mocé-Llivina L., Muniesa M., Pimenta-Vale H., Lucena F., Jofre J., Moce L., Muniesa M., Pimenta-Vale H., Lucena F., Jofre J. Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Appl. Environ. Microbiol. 2003, 69:1452-1456. 10.1128/AEM.69.3.1452.
42. Muniesa M., Blanch A.R., Lucena F., Jofre J. Bacteriophages may bias outcome of bacterial enrichment cultures. Appl. Environ. Microbiol. 2005, 71:4269-4275.
43. Nielsen K.M., Johnsen P.J., Bensasson D., Daffonchio D. Release and persistence of extracellular DNA in the environment. Environ. Biosafety Res. 2007, 6:37-53. 10.1051/ebr:2007031.
44. Norman J.M., Handley S., a, Parkes, M., Virgin H.W., Norman J.M., Handley S.A., Baldridge M.T., Droit L., Liu C.Y., Keller B.C. Disease-specific alterations in the enteric virome in article disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 2015, 160:447-460. 10.1016/j.cell.2015.01.002.
45. Pietramellara G., Ascher J., Borgogni F., Ceccherini M.T., Guerri G., Nannipieri P. Extracellular DNA in soil and sediment: fate and ecological relevance. Biol. Fertil. Soils 2009, 45:219-235. 10.1007/s00374-008-0345-8.
46. Quirós P., Colomer-Lluch M., Martínez-Castillo A., Miró E., Argente M., Jofre J., Navarro F., Muniesa M. Antibiotic resistance genes in the bacteriophage DNA fraction of human fecal samples. Antimicrob. Agents Chemother. 2014, 58:606-609. 10.1128/AAC.01684-13.
47. Rodriguez-Mozaz S., Chamorro S., Marti E., Huerta B., Gros M., Sànchez-Melsió A., Borrego C.M., Barceló D., Balcázar J.L. Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res. 2014, 69C:234-242. 10.1016/j.watres.2014.11.021.
48. Romanowski G., Lorenz M.G., Sayler G., Wackernagel W. Persistence of free plasmid DNA in soil monitored by various methods, including a transformation assay. Appl. Environ. Microbiol. 1992, 58:3012-3019.
49. Sharp D.G., Hook A.E., Taylor A.R., Beard D., Beard J.W. Sedimentarion characters and pH stability of the T2 bacteriophage of Escherichia coli. J. Biol. Chem. 1946, 165:259-270.
50. Horizontal Gene Transfer 2002, Academic Press, San Diego. second ed. M. Syvanen, C.I. Kado (Eds.).
51. The White House National Strategy for Combating Antibiotic- Resistant 2014.
52. Wommack K.E., Hill R.T., Muller T.A., Colwell R.R. Effects of sunlight on bacteriophage viability and structure. Appl. Environ. Microbiol. 1996, 62:1336-1341.
53. World Health Organization Antimicrobial Resistance 2014, Global Report on Surveillance 2014, (Geneva).
54. Xu J., Xu Y., Wang H., Guo C., Qiu H., He Y., Zhang Y., Li X., Meng W. Occurrence of antibiotics and antibiotic resistance genes in a sewage treatment plant and its effluent-receiving river. Chemosphere 2014, 119:1379-1385. 10.1016/j.chemosphere.2014.02.040.
55. Yuan Q.-B., Guo M.-T., Yang J. Fate of antibiotic resistant bacteria and genes during wastewater chlorination: implication for antibiotic resistance control. PLoS One 2015, 10:e0119403. 10.1371/journal.pone.0119403.
56. Zhang Y., Marrs C.F., Simon C., Xi C. Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci. Total Environ. 2009, 407:3702-3706. 10.1016/j.scitotenv.2009.02.013.
57. Zhang Y., Zhuang Y., Geng J., Ren H., Zhang Y., Ding L., Xu K. Inactivation of antibiotic resistance genes in municipal wastewater effluent by chlorination and sequential UV/chlorination disinfection. Sci. Total Environ. 2015, 512-513:125-132. 10.1016/j.scitotenv.2015.01.028.
58. Zhuang Y., Ren H., Geng J., Zhang Y., Zhang Y., Ding L., Xu K. Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environ. Sci. Pollut. Res. Int. 2014, 10.1007/s11356-014-3919-z.