Minimal selective concentrations of tetracycline in complex aquatic bacterial biofilms

Science of the Total Environment

Volumn 553, Issue , 2016, Pages 587-595

  Lundström, Sara V ^a   Östman, Marcus ^b   Bengtsson Palme, Johan ^a   Rutgersson, Carolin ^a   Thoudal, Malin ^a   Sircar, Triranta ^c   Blanck, Hans ^c   Eriksson, K Martin ^d   Tysklind, Mats ^b   Flach, Carl Fredrik ^a   Larsson, D G Joakim ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Antibiotic contaminants; Antibiotic resistance; Environmental emission limits; Minimal selective concentration; Risk assessment

Indexed keywords

ANIMALS; ANTIBIOTICS; BACTERIA; BIOFILMS; FLOWCHARTING; GENES; RISK ASSESSMENT; SEWAGE TREATMENT PLANTS; VETERINARY MEDICINE;

ANTIBIOTIC CONTAMINANTS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; ANTIBIOTIC-RESISTANT BACTERIA; ENVIRONMENTAL EMISSIONS; METAGENOMIC ANALYSIS; SELECTIVE CONCENTRATION; TAXONOMIC COMPOSITION;

AQUATIC ORGANISMS;

TETRACYCLINE; WATER POLLUTANT;

ANTIBIOTIC RESISTANCE; ANTIBIOTICS; BACTERIUM; BIOFILM; CONCENTRATION (COMPOSITION); GENE; RISK ASSESSMENT;

ACIDOVORAX; ACINETOBACTER; AEROMONAS; ALCALIGENACEAE; ARTICLE; BACTERIAL GENE; BIOFILM; CAULOBACTERACEAE; CMLA GENE; CONTROLLED STUDY; DYELLA; EXIGUOBACTERIUM; FLOR GENE; GENOTYPE; METAGENOMICS; MICROBIAL COMMUNITY; MPHA GENE; NONHUMAN; PHENOTYPE; POPULATION ABUNDANCE; PRIORITY JOURNAL; PSEUDOMONAS; RHODOBACTERACEAE; RISK ASSESSMENT; SEWAGE TREATMENT PLANT; SPHINGOMONADALES; SUL1 GENE; TAXONOMIC IDENTIFICATION; TETA GENE; TETG GENE; WATER POLLUTION; ANALYSIS; ANTIBIOTIC RESISTANCE; BACTERIUM; ENVIRONMENTAL MONITORING; GENETICS; GROWTH, DEVELOPMENT AND AGING; WATER POLLUTANT;

ANIMALIA; BACTERIA (MICROORGANISMS);

BACTERIA; BIOFILMS; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL MONITORING; TETRACYCLINE; TETRACYCLINE RESISTANCE; WATER POLLUTANTS, CHEMICAL;

EID: 84960875881     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2016.02.103     Document Type: Article

References (46)

1. Agersø Y., Guardabassi L. Identification of Tet 39, a novel class of tetracycline resistance determinant in Acinetobacter spp. of environmental and clinical origin. J. Antimicrob. Chemother. 2005, 55(4):566-569.
2. Ågerstrand M., Berg C., Björlenius B., Breitholtz M., Brunström B., Fick J., Gunnarsson L., Larsson D.G.J., Sumpter J.P., Tysklind M., Rudén C. Improving environmental risk assessment of human pharmaceuticals. Environ. Sci. Technol. 2015, 49(9):5336-5345.
3. Agwuh K.N., MacGowan A. Pharmacokinetics and pharmacodynamics of the tetracyclines including glycylcyclines. J. Antimicrob. Chemother. 2006, 58:256-265.
4. Andersson D.I., Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 2014, 12:465-478.
5. Ashbolt N.J., Amezquita A., Backhaus T., Borriello P., Brandt K.K., Collignon P., Coors A., Finley R., Gaze W.H., Heberer T., Lawrence J.R., Larsson D.G.J., McEwen S.A., Ryan J.J., Schönfeld J., Silley P., Snape J.R., Van den Eede C., Topp E. Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 2013, 121(9):993-1001.
6. Bai Y., Meng W., Xu J., Zhang Y., Guo C. Occurrence, distribution and bioaccumulation of antibiotics in the Liao River Basin in China. Environ. Sci. Processes Impacts 2014, 16(3):586-593.
7. Bengtsson-Palme J., Larsson D.G.J. Antibiotic resistance genes in the environment: prioritizing risks. Nat. Rev. Microbiol. 2015, 13(6):396.
8. Bengtsson-Palme J., Larsson D.G.J. Concentrations of antibiotics predicted to select for resistant bacteria: proposed limits for environmental regulation. Environ. Int. 2016, 86:140-149.
9. Bengtsson-Palme J., Boulund F., Fick J., Kristiansson E., Larsson D.G.J. Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front. Microbiol. 2014, 5:648.
10. Bengtsson-Palme J., Hartmann M., Eriksson K.M., Pal C., Thorell K., Larsson D.G.J., Nilsson R.H. Metaxa2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol. Ecol. Resour. 2015, 15(6):1403-1414.
11. Bengtsson-Palme J., Angelin M., Huss M., Kjellqvist S., Kristiansson E., Palmgren H., Larsson D.G.J., Johansson A. The human gut microbiome as a transporter of antibiotic resistance genes between continents. Antimicrob. Agents Chemother. 2015, 59(6):6551-6560.
12. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995, 57:289-300.
13. Berg J., Brandt K.K., Al-Soud W.A., Holm P.E., Hansen L.H., Sorensen S.J., Nybroe O. Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl. Environ. Microbiol. 2012, 78(20):7438-7446.
14. Blanck H. A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Hum. Ecol. Risk. Assess. 2002, 8(5):1003-1034.
15. Brandt K.K., Amézquita A., Backhaus T., Boxall A., Coors A., Heberer T., Lawrence J.R., Lazorchak J., Schönfeld J., Snape J.R., Zhu Y.G., Topp E. Ecotoxicological assessment of antibiotics: a call for improved consideration of microorganisms. Environ. Int. 2015, 10.1016/j.envint.2015.09.013.
16. Brosche S., Backhaus T. Toxicity of five protein synthesis inhibiting antibiotics and their mixture to limnic bacterial communities. Aquat. Toxicol. 2010, 99(4):457-465.
17. Coenen S., Adriaenssens N., Versporten A., Muller A., Minalu G., Faes C., Vankerckhoven V., Aerts M., Hens N., Molenberghs G., Goossens H., ESAC Project Group European surveillance of antimicrobial consumption (ESAC): outpatient use of tetracyclines, sulphonamides and trimethoprim, and other antibacterials in Europe (1997-2009). J. Antimicrob. Chemother. 2011, 66(6):vi57-vi70.
18. Davies J., Davies D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 2010, 74(3):417-433.
19. D'Costa V.M., King C.E., Kalan L., Morar M., Sung W.W.L., Schwarz C., Froese D., Zazula G., Calmels F., Debruyne R., Golding G.B., Poinar H.N., Wright G.D. Antibiotic resistance is ancient. Nature 2011, 477(7365):457-461.
20. Elmund G.K., Morrison S.M., Grant D.W., Nevins S.M. Role of excreted chlortetracycline in modifying the decomposition process in feedlot waste. Bull. Environ. Contam. Toxicol. 1971, 6(2):129-132.
21. Gullberg E., Cao S., Berg O.G., Ilback C., Sandberg L., Hughes D., Andersson D.I. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 2011, 7(7).
22. Hill A.B. The environment and disease: association or causation?. Proc. R. Soc. Med. 1965, 58:295-300.
23. Høiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35:322-332.
24. Huang K., Tang J., Zhang X.-X., Xu K., Ren H. A comprehensive insight into tetracycline resistant bacteria and antibiotic resistance gene in activated sludge using next-generation sequencing. Int. J. Mol. Sci. 2014, 15(6):10083-10100.
25. Jutkina L., Rutgersson C., Flach C.-F., Larsson D.G.J. An assay for determining minimal concentrations of antibiotics that drive horizontal transfer of resistance. Sci. Total Environ. 2016, 548-549:131-138.
26. Karthikeyan K.G., Meyer M.T. Occurrence of antibiotics in wastewater treatment facilities in Wisconsin, USA. Sci. Total Environ. 2006, 361:196-207.
27. Kelly J.J., Minalt N., Culotti A., Pryor M., Packman A. Temporal variations in the abundance and composition of biofilm communities colonizing drinking water distribution pipes. PLoS One 2014, 9(5).
28. 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 US streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 2002, 36(6):1202-1211.
29. Kools S.A., Moltmann J.F., Knacker T. Estimating the use of veterinary medicines in the European Union. Regul. Toxicol. Pharmacol. 2008, 50(1):59-65.
30. Larsson D.G.J. Pollution from drug manufacturing: review and perspectives. Philos. Trans. R. Soc. B 2014, 369:20130571.
31. Lindberg R.H., Ostman M., Olofsson U., Grabic R., Fick J. Occurrence and behavior of 105 active pharmaceutical ingredients in sewage waters of a municipal sewer collection system. Water Res. 2014, 58:221-229.
32. Liu A., Fong A., Becket E., Yuan J., Tamae C., Medrano L., Maiz M., Wahba C., Lee C., Lee K., Tran K.P., Yang H., Hoffman R.M., Salih A., Miller J.H. Selective advantage of resistant strains at trace levels of antibiotics: a simple and ultrasensitive color test for detection of antibiotics and genotoxic agents. Antimicrob. Agents Chemother. 2011, 55(3):1204-1210.
33. Martinez J.L., Coque T.M., Baquero F. What is a resistance gene? Ranking risk in resistomes. Nat. Rev. Microbiol. 2015, 13:116-123.
34. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59(3):695-700.
35. Oksanen J., Blanchet F.G., Kindt R., Legendre P., Minchin P.R., OHara R.B., Simpson G.L., Solymos P., Stevens M.H.H., Wagner H. Vegan: Community Ecology Package 2011.
36. Pruden A., Larsson D.G.J., Amézquita A., Collignon P., Brandt K.K., Graham D.W., Lazorchak J.M., Suzuki S., Silley P., Snape J.R., Topp E., Zhang T., Zhu Y.G. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ. Health Perspect. 2013, 121(8):878-885.
37. Quinlan E.L., Nietch C.T., Blocksom K., Lazorchak J.M., Batt A.L., Griffiths R., Klemm D.J. Temporal dynamics of periphyton exposed to tetracycline in stream mesocosms. Environ. Sci. Technol. 2011, 45(24):10684-10690.
38. Rizzo L., Manaia C., Merlin C., Schwartz T., Dagot C., Ploy M.C., Michael I., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 2013, 447:345-360.
39. Ruiz-González C., Lefort T., Massana R., Simó R., Gasol J.M. Diel changes in bulk and single-cell bacterial heterotrophic activity in winter surface waters of the northwestern Mediterranean Sea. Limnol. Oceanogr. 2012, 57(1):29-42.
40. Sassman S.A., Lee L.S. Sorption of three tetracyclines by several soils: assessing the role of pH and cation exchange. Environ. Sci. Technol. 2005, 39(19):7452-7459.
41. Segura P.A., Francois M., Gagnon C., Sauve S. Review of the occurrence of anti-infectives in contaminated wastewaters and natural and drinking waters. Environ. Health Perspect. 2009, 117(5):675-684.
42. Szczepanowski R., Linke B., Krahn I., Gartemann K.-H., Gützkow T., Eichler W., Pühler A., Schlüter A. Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 2009, 155:2306-2319.
43. Topal M., Arslan Topal E.I. Investigation of tetracycline and degradation products in Euphrates river receiving outflows of trout farms. Aquac. Res. 2015, 10.1111/are.12834.
44. Watkinson A.J., Murby E.J., Kolpin D.W., Costanzo S.D. The occurrence of antibiotics in an urban watershed: from wastewater to drinking water. Sci. Total Environ. 2009, 407(8):2711-2723.
45. Ye L., Zhang T. Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing. Appl. Microbiol. Biotechnol. 2013, 97:2681-2690.
46. Yin J., Zhang X.-X., Wu B., Xian Q. Metagenomic insights into tetracycline effects on microbial community and antibiotic resistance of mouse gut. Ecotoxicology 2015, 10.1007/s10646-015-1540-7.