Effects on groundwater microbial communities of an engineered 30-day in situ exposure to the antibiotic sulfamethoxazole

Environmental Science and Technology

Volumn 46, Issue 14, 2012, Pages 7478-7486

  Haack, Sheridan K ^a   Metge, David W ^a   Fogarty, Lisa R ^a   Meyer, Michael T ^a   Barber, Larry B ^a   Harvey, Ronald W ^a   Leblanc, Denis R ^a   Kolpin, Dana W ^a  

^a U S GEOLOGICAL SURVEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SULFAMETHOXAZOLE; BACTERIAL COMMUNITY; CLASS I; CLINICAL APPLICATION; COMMUNITY COMPOSITION; DOSE RESPONSE; ECOLOGICAL FUNCTIONS; ENVIRONMENTAL EXPOSURE; FILTER CHAMBER; IN-SITU; INTEGRONS; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY STRUCTURES; ORDERS OF MAGNITUDE; PSEUDOMONAS STUTZERI; RESISTANT BACTERIA; SULFAMETHOXAZOLE; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

ANTIBIOTICS; AQUIFERS; GENE ENCODING; GROUNDWATER RESOURCES; MICROORGANISMS;

GROUNDWATER POLLUTION;

BROMIDE; GROUND WATER; SULFAMETHOXAZOLE; SULFONAMIDE;

ANTIBIOTIC RESISTANCE; ANTIBIOTICS; AQUIFER; BACTERIUM; COMMUNITY DYNAMICS; CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; ECOSYSTEM FUNCTION; EXPERIMENTAL STUDY; GROUNDWATER POLLUTION; IN SITU MEASUREMENT; INHIBITION; MICROBIAL COMMUNITY; MORTALITY; OLIGOTROPHIC ENVIRONMENT; WATER QUALITY;

ACCLIMATIZATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EXPOSURE; ECOLOGY; ENTEROBACTER; EXPOSURE; FILTER; GENE MUTATION; GROWTH INHIBITION; INTEGRON; MICROBIAL COMMUNITY; MICROBIAL GROWTH; MORTALITY; PHYLOGENY; PSEUDOMONAS STUTZERI; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEWAGE;

ACCLIMATIZATION; ANTI-BACTERIAL AGENTS; BACTERIA; BROMIDES; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL EXPOSURE; GROUNDWATER; MICROBIAL CONSORTIA; MICROBIAL VIABILITY; NEW HAMPSHIRE; PRINCIPAL COMPONENT ANALYSIS; SULFAMETHOXAZOLE; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS STUTZERI;

EID: 84863936004     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es3009776     Document Type: Article

References (37)

1. Glassmeyer, S. T.; Furlong, E. T.; Kolpin, D. W.; Cahill, J. D.; Zaugg, S. D.; Werner, S. L.; Meyer, M. T.; Kryak, D. D. Transport of chemical and microbial compounds from known wastewater discharges: Potential for use as indicators of human fecal contamination Environ. Sci. Technol. 2005, 39, 5157-5169
2. Peng, X.; Wang, Z.; Kuang, W.; Tan, J.; Li, K. A preliminary study on the occurrence and behavior of sulfonamides, ofloxacin and chloramphenicol antimicrobials in wastewaters of two sewage treatment plants in Guangzhou, China Sci. Total Environ. 2006, 371, 314-322
3. Zorita, S.; Mårtensson, L.; Mathiasson, L. Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the south of Sweden Sci. Total Environ. 2009, 407, 2760-2770
4. Siemens, J.; Huschek, G.; Siebe, C.; Kaupenjohann, M. Concentrations and mobility of human pharmaceuticals in the worlds largest wastewater irrigation system, Mexico City-Mezquital Valley Water Res. 2008, 42, 2124-2134
5. Gulkowska, A.; Leung, H. W.; So, M. K.; Taniyasu, S.; Yamashita, N.; Yeung, L.; Richardson, B. J.; Lei, A. P.; Giesy, J. P.; Lam, P. K. S. Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China Water Res. 2008, 42, 395-403
6. Barnes, K. K.; Kolpin, D. W.; Furlong, E. T.; Zaugg, S. D.; Meyer, M. T.; Barber, L. B. A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States-I) Groundwater Sci. Total Environ. 2008, 402, 192-200
7. Barber, L. B.; Keefe, S. H.; Leblanc, D. R.; Bradley, P. M.; Chapelle, F. H.; Meyer, M. T.; Loftin, K. A.; Kolpin, D. W.; Rubio, F. Fate of sulfamethoxazole, 4-nonylphenol, and 17beta-estradiol in groundwater contaminated by wastewater treatment plant effluent Environ. Sci. Technol. 2009, 43, 4843-4850
8. Snyder, S. A.; Leising, J.; Westerhoff, P.; Yoon, Y.; Mash, H.; Vanderford, B. Biological and physical attenuation of endocrine disrupters and pharmaceuticals: Implications for water reuse Groundwater Monit. Remed. 2004, 24, 108-118
9. Kolpin, D. W.; Furlong, E. T.; Meyer, M. T.; Thurman, E. M.; Zaugg, S. D.; Barber, L. B.; Buxton, H. T. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. Streams, 1999-2000: A national reconnaissance Environ. Sci. Technol. 2002, 36, 1202-1211
10. Kümmerer, K. (ed.) Pharmaceuticals in the Environment: Sources, Fate, Effects and Risks; Springer: Berlin.
11. Antimicrobial Resistance in Bacteria of Animal Origin; Aarestrup, F. M., Ed.; ASM Press: Washington, DC, 2006.
12. Brown, M. G.; Balkwill, D. L. Antibiotic resistance in bacteria isolated from the deep terrestrial subsurface Microb. Ecol. 2009, 57, 484-493
13. Gullberg, E.; Cao, S.; Berg, O. G.; Ilbäck, C.; Sandegren, L.; Hughes, D.; Andersson, D. I. Selection of resistant bacteria at very low antibiotic concentrations PloS Pathog. 2011, 7, e1002158
14. Underwood, J. C.; Harvey, R. W.; Metge, D. W.; Repert, D. A.; Baumgartner, L. K.; Smith, R. L.; Roane, T. M.; Barber, L. B. Effects of the antimicrobial sulfamethoxazole on groundwater bacterial enrichment Environ. Sci. Technol. 2011, 45, 3096-3101
15. Clinical Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twelfth Informational Supplement, M-100-S12, 2002; Vol. 22.
16. Levin, B. R.; Rozen, D. E. Non-inherited antibiotic resistance Nat. Rev. Microbiol. 2006, 4, 556-562
17. Lévesque, C.; Piché, L.; Larose, C.; Roy, P. H. PCR mapping of integrons reveals several novel combinations of resistance genes Antimicrob. Agents Chemother. 1995, 38 (1) 185-191
18. Tenover, F. C. Mechanisms of antimicrobial resistance in bacteria Am. J. Med. 2006, 119, S3-S10
19. LeBlanc, D. R. Sewage Plume in a Sand and Gravel Aquifer, Cape Cod, Massachusetts; U.S. Geological Survey Water Supply Paper, 2218, 1984.
20. Repert, D. A.; Barber, L. B.; Hess, K. M.; Keefe, S. H.; Kent, D. B.; LeBlanc, D. R.; Smith, R. L. Long-term natural attenuation of carbon and nitrogen within a groundwater plume after removal of the treated wastewater source Environ. Sci. Technol. 2006, 40, 1154-1162
21. Harvey, R. W.; George, L. H. Growth determinations for unattached bacteria in a contaminated aquifer Appl. Environ. Microbiol. 1987, 53, 2992-2996
22. Metge, D. W.; Brooks, M.; Smith, R.; Harvey, R. W. Effect of treated-sewage contamination upon bacterial energy charge, adenine nucleotides, and DNA in a sandy aquifer on Cape Cod Appl. Environ. Microbiol. 1993, 59, 2304-2310
23. Lisle, J. T.; Harvey, R. W.; Aiken, G. R.; Metge, D. W. Microbial and geochemical Investigations of Dissolved Organic Carbon and Microbial Ecology of Native Waters from the Biscayne and Upper Floridan Aquifers; U.S. Geological Survey Open-File Report 2010-1021, 2010, 33.
24. Kinner, N. E.; Harvey, R. W.; Blakeslee, K.; Novarino, G.; Meeker, L. D. Size-selective predation on groundwater bacteria by nanoflagellates in an organic-contaminated aquifer Appl. Environ. Microbiol. 1998, 64, 618-625
25. Harvey, R. W.; Garabedian, S. P. Use of colloid filtration theory in modeling movement of bacteria through a contaminated sandy aquifer Environ. Sci. Technol. 1991, 25, 178-185
26. Becker, M. W.; Metge, D. W.; Collins, S. A.; Shapiro, A. M.; Harvey, R. W. Bacterial transport experiments in fractured crystalline bedrock Ground Water 2003, 41, 682-689
27. Harvey, R. W.; Metge, D. W.; Mohanram, A.; Gao, X.; Chorover, J. Differential effects of anionic and nonionic surfactants upon re-entrainment of groundwater bacteria and bacteria-sized microspheres during transport through a contaminated, sandy aquifer Environ. Sci. Technol. 2011, 45, 3252-3259
28. Amy, P. S.; Haldeman, D. L.; Ringelberg, D.; Hall, D. H.; Russell, C. Comparison of identification systems for classification of bacteria isolated from water and endolithic habitats within the deep subsurface Appl. Environ. Microbiol. 1992, 58, 3367-3373
29. Finney, D. J. Probit Analysis; Cambridge University Press: Cambridge, England, 1952.
30. Schütte, U. M. E.; Abdo, Z.; Bent, S. J.; Shyu, C.; Williams, C. J.; Pierson, J. D.; Forney, L. J. Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities Appl. Microbiol. Biotechnol. 2008, 80, 365-380
31. Smith, C. J.; Danilowicz, B. S.; Clear, A. K.; Costello, F. J.; Wilson, B.; Meijer, W. G. T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles FEMS Microbiol. Ecol. 2005, 54, 375-380
32. Kent, A. D.; Smith, D. J.; Benson, B. J.; Triplett, E. W. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities Appl. Environ. Microbiol. 2003, 69, 6768-6776
33. Schumann, R.; Schiewer, U.; Karsten, U.; Rieling, T. Viability of bacteria from different aquatic habitats. II. Cellular fluorescent markers for membrane integrity and metabolic activity Aquat. Microb. Ecol. 2003, 32, 137-150
34. Ericsson, M.; Hanstorp, D.; Hagberg, P.; Enger, J.; Nyström, T. Sorting out bacterial viability with optical tweezers J. Bacteriol. 2000, 182, 5551-5555
35. Oliver, J. D. The viable but nonculturable state in bacteria J. Microbiol. 2005, 43 (Spec No) 93-100
36. Hazendaroglu, B. Z.; Yates, M. V.; Maduro, M. F.; Walker, S. L. Effects of residual antibiotics in groundwater on Salmonella typhimurium: Changes in antibiotic resistance, in vivo and in vitro pathogenicity J. Environ. Monit. 2012, 14, 41-47
37. Wright, G. D. The antibiotic resistome: The nexus of chemical and genetic diversity Nat. Rev. Microbiol. 2007, 5, 175-186