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Impact of primary carbon sources on microbiome shaping and biotransformation of pharmaceuticals and personal care products

  • Karen Rossmassler
  • Sunah Kim
  • Corey D. Broeckling
  • Sarah Galloway
  • Jessica Prenni
  • Susan K. De LongEmail author
Original Paper

Abstract

Knowledge of the conditions that promote the growth and activity of pharmaceutical and personal care product (PPCP)-degrading microorganisms within mixed microbial systems are needed to shape microbiomes in biotreatment reactors and manage process performance. Available carbon sources influence microbial community structure, and specific carbon sources could potentially be added to end-of-treatment train biotreatment systems (e.g., soil aquifer treatment [SAT]) to select for the growth and activity of a range of microbial phylotypes that collectively degrade target PPCPs. Herein, the impacts of primary carbon sources on PPCP biodegradation and microbial community structure were explored to identify promising carbon sources for PPCP biotreatment application. Six types of primary carbon sources were investigated: casamino acids, two humic acid and peptone mixtures (high and low amounts of humic acid), molasses, an organic acids mixture, and phenol. Biodegradation was tracked for five PPCPs (diclofenac, 5-fluorouracil, gemfibrozil, ibuprofen, and triclosan). Primary carbon sources were found to differentially impact microbial community structures and rates and efficiencies of PPCP biotransformation. Of the primary carbon sources tested, casamino acids, organic acids, and phenol showed the fastest biotransformation; however, on a biomass-normalized basis, both humic acid-peptone mixtures showed comparable or superior biotransformation. By comparing microbial communities for the different primary carbon sources, abundances of unclassified Beijerinckiaceae, Beijerinckia, Sphingomonas, unclassified Sphingomonadaceae, Flavobacterium, unclassified Rhizobiales, and Nevskia were statistically linked with biotransformation of specific PPCPs.

Keywords

Biodegradation Biotransformation Carbon source Pharmaceuticals and personal care products Trace organic contaminants Next-generation sequencing 

Notes

Acknowledgements

We sincerely thank Rhodes Trussell, Sangam Stanczak and Yan Qu of Trussell Technologies for providing soil aquifer treatment column material. We would also like to thank Link Mueller for providing activated sludge samples. We wish to thank the Franklin Graybill Statistical Laboratory at Colorado State University of statistical consulting. This research was funded by the Colorado State University Water Center, and other internal funds.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10532_2019_9871_MOESM1_ESM.docx (2.5 mb)
Supplementary material 1 (DOCX 2570 kb)

References

  1. Alidina M, Li D, Ouf M, Drewes JE (2014) Role of primary substrate composition and concentration on attenuation of trace organic chemicals in managed aquifer recharge systems. J Environ Manage 144:58–66.  https://doi.org/10.1016/j.jenvman.2014.04.032 CrossRefPubMedGoogle Scholar
  2. Alidina M, Shewchuk J, Drewes JE (2015) Effect of temperature on removal of trace organic chemicals in managed aquifer recharge systems. Chemosphere 122:23–31.  https://doi.org/10.1016/j.chemosphere.2014.10.064 CrossRefPubMedGoogle Scholar
  3. Alvarino T, Suarez S, Lema JM, Omil F (2014) Understanding the removal mechanisms of PPCPs and the influence of main technological parameters in anaerobic UASB and aerobic CAS reactors. J Hazard Mater 278:506–513.  https://doi.org/10.1016/j.jhazmat.2014.06.031 CrossRefPubMedGoogle Scholar
  4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interations with plants and other organisms. Annu Rev Plant Biol 57:233–266.  https://doi.org/10.1146/annurev.arplant.57.032905.105159 CrossRefPubMedGoogle Scholar
  5. Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192.  https://doi.org/10.1016/s0038-0717(03)00179-2 CrossRefGoogle Scholar
  6. Benner J et al (2013) Is biological treatment a viable alternative for micropollutant removal in drinking water treatment processes? Water Res 47:5955–5976.  https://doi.org/10.1016/j.watres.2013.07.015 CrossRefPubMedGoogle Scholar
  7. Brown JC, Snoeyink VL, Raskin L, Lin R (2003) The sensitivity of fixed-bed biological perchlorate removal to changes in operating conditions and water quality characteristics. Water Res 37:206–214CrossRefPubMedGoogle Scholar
  8. Carvalho MDF, Ferreira MIM, Moreira IS, Castro PML, Janssen DB (2007) Degradation of fluorobenzene by a Rhizobiales strain F11 via ortho cleavage of 4-fluorocatechol and catechol. J Biotechnol 131:S249–S249.  https://doi.org/10.1016/j.jbiotec.2007.07.451 CrossRefGoogle Scholar
  9. Chubukov V, Gerosa L, Kochanowski K, Sauer U (2014) Coordination of microbial metabolism. Nat Rev Microbiol 12:327–340.  https://doi.org/10.1038/nrmicro3238 CrossRefPubMedGoogle Scholar
  10. Cole JR et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145.  https://doi.org/10.1093/nar/gkn879 CrossRefPubMedGoogle Scholar
  11. Comte A et al (2013) Biochemical, transcriptional and translational evidences of the phenol-meta-degradation pathway by the hyperthermophilic Sulfolobus solfataricus 98/2. PLoS ONE 8:8.  https://doi.org/10.1371/journal.pone.0082397 CrossRefGoogle Scholar
  12. Da Silva MLB, Daprato RC, Gomez DE, Hughes JB, Ward CH, Alvarez PJJ (2006) Comparison of bioaugmentation and biostimulation for the enhancement of dense nonaqueous phase liquid source zone bioremediation. Water Environ Res 78:2456–2465.  https://doi.org/10.2175/106143006x123111 CrossRefPubMedGoogle Scholar
  13. Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107:907–938.  https://doi.org/10.2307/3434573 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dedysh SN, Smirnova KV, Khmelenina VN, Suzina NE, Liesack W, Trotsenko YA (2005) Methylotrophic autotrophy in Beijerinckia mobilis. J Bacteriol 187:3884–3888.  https://doi.org/10.1128/jb.187.11.3884-3888.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Domaradzka D, Guzik U, Hupert-Kocurek K, Wojcieszynska D (2015) Cometabolic degradation of naproxen by Planococcus sp strain S5. Water Air Soil Pollut.  https://doi.org/10.1007/s11270-015-2564-6 PubMedPubMedCentralGoogle Scholar
  16. Du K, Zhou B, Yuan R (2017) Biodegradation of 2-methylisoborneol by single bacterium in culture media and river water environment. Int J Environ Stud 74:399–411CrossRefGoogle Scholar
  17. Espejo A, Aguinaco A, Amat AM, Beltran FJ (2014) Some ozone advanced oxidation processes to improve the biological removal of selected pharmaceutical contaminants from urban wastewater. J Environ Sci Health, Part A 49:410–421.  https://doi.org/10.1080/10934529.2014.854652 CrossRefGoogle Scholar
  18. Gerrity D, Gamage S, Holady JC, Mawhinney DB, Quinones O, Trenholm RA, Snyder SA (2011) Pilot-scale evaluation of ozone and biological activated carbon for trace organic contaminant mitigation and disinfection. Water Res 45:2155–2165.  https://doi.org/10.1016/j.watres.2010.12.031 CrossRefPubMedGoogle Scholar
  19. Gerrity D, Owens-Bennett E, Venezia T, Stanford BD, Plumlee MH, Debroux J, Trussell RS (2014) Applicability of ozone and biological activated carbon for potable reuse. Ozone-Sci Eng 36:123–137.  https://doi.org/10.1080/01919512.2013.866886 CrossRefGoogle Scholar
  20. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9Google Scholar
  21. Hay AG, Dees PM, Sayler GS (2001) Growth of a bacterial consortium on triclosan. Fems Microbiol Ecol 36:105–112.  https://doi.org/10.1111/j.1574-6941.2001.tb00830.x CrossRefPubMedGoogle Scholar
  22. Jones-Lepp TL, Sanchez C, Alvarez DA, Wilson DC, Taniguchi-Fu RL (2012) Point sources of emerging contaminants along the Colorado River Basin: source water for the arid Southwestern United States. Sci Total Environ 430:237–245.  https://doi.org/10.1016/j.scitotenv.2012.04.053 CrossRefPubMedGoogle Scholar
  23. Kahl S, Kleinsteuber S, Nivala J, van Afferden M, Reemtsma T (2018) Emerging biodegradation of the previously persistent artificial sweetener acesulfame in biological wastewater treatment. Environ Sci Technol 52:2717–2725.  https://doi.org/10.1021/acs.est.7b05619 CrossRefPubMedGoogle Scholar
  24. Kim S, Rossmassler K, Broeckling CD, Galloway S, Prenni J, De Long SK (2017) Impact of inoculum sources on biotransformation of pharmaceuticals and personal care products. Water Res 125:227–236.  https://doi.org/10.1016/j.watres.2017.08.041 CrossRefPubMedGoogle Scholar
  25. Kjeldal H, Zhou NA, Wissenbach DK, von Bergen M, Gough HL, Nielsen JL (2016) Genomic, proteomic, and metabolite characterization of gemfibrozil-degrading organism Bacillus sp. GeD10. Environ Sci Technol 50:744–755.  https://doi.org/10.1021/acs.est.5b05003 CrossRefPubMedGoogle Scholar
  26. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120.  https://doi.org/10.1128/aem.01043-13 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lahti M, Oikari A (2011) Microbial transformation of pharmaceuticals naproxen, bisoprolol, and diclofenac in aerobic and anaerobic environments. Arch Environ Contamin Toxicol 61:202–210.  https://doi.org/10.1007/s00244-010-9622-2 CrossRefGoogle Scholar
  28. Leandro T, Franca L, Nobre MF, Schumann P, Rossello-Mora R, da Costa MS (2012) Nevskia aquatilis sp nov and Nevskia persephonica sp nov., isolated from a mineral water aquifer and the emended description of the genus Nevskia. Syst Appl Microbiol 35:297–301.  https://doi.org/10.1016/j.syapm.2012.05.001 CrossRefPubMedGoogle Scholar
  29. Lee PKH, Macbeth TW, Sorenson KS, Deeb RA, Alvarez-Cohen L (2008) Quantifying genes and transcripts to assess the in situ physiology of “Dehalococcoides” spp. in a trichloroethene-contaminated groundwater site. Appl Environ Microbiol 74:2728–2739.  https://doi.org/10.1128/aem.02199-07 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lee CO, Howe KJ, Thomson BM (2012) Ozone and biofiltration as an alternative to reverse osmosis for removing PPCPs and micropollutants from treated wastewater. Water Res 46:1005–1014.  https://doi.org/10.1016/j.watres.2011.11.069 CrossRefPubMedGoogle Scholar
  31. Leisinger T, Bader R, Hermann R, Schmid-Appert M, Vuilleumier S (1994) Microbes, enzymes and genes involved in dichloromethane utilization. Biodegradation 5:237–248.  https://doi.org/10.1007/bf00696462 CrossRefPubMedGoogle Scholar
  32. Li D, Alidina M, Drewes JE (2014) Role of primary substrate composition on microbial community structure and function and trace organic chemical attenuation in managed aquifer recharge systems. Appl Microbiol Biotechnol 98:5747–5756.  https://doi.org/10.1007/s00253-014-5677-8 CrossRefPubMedGoogle Scholar
  33. Lo KV, Zhu CM, Cheuk W (1998) Biodegradation of pentachlorophenol by Flavobacterium species in batch and immobilized continuous reactors. Environ Technol 19:91–96CrossRefGoogle Scholar
  34. Macedo AJ, Timmis KN, Abraham WR (2007) Widespread capacity to metabolize polychlorinated biphenyls by diverse microbial communities in soils with no significant exposure to PCB contamination. Environ Microbiol 9:1890–1897.  https://doi.org/10.1111/j.462-2920.2007.01305.x CrossRefPubMedGoogle Scholar
  35. Margot J et al (2013) Treatment of micropollutants in municipal wastewater: ozone or powdered activated carbon? Sci Total Environ 461:480–498.  https://doi.org/10.1016/j.scitotenv.2013.05.034 CrossRefPubMedGoogle Scholar
  36. Murdoch RW, Hay AG (2005) Formation of catechols via removal of acid side chains from ibuprofen and related aromatic acids. Appl Environ Microbiol 71:6121–6125.  https://doi.org/10.1128/aem.71.10.6121-6125.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Onesios KM, Bouwer EJ (2012) Biological removal of pharmaceuticals and personal care products during laboratory soil aquifer treatment simulation with different primary substrate concentrations. Water Res 46:2365–2375.  https://doi.org/10.1016/j.watres.2012.02.001 CrossRefPubMedGoogle Scholar
  38. Onesios KM, Yu JT, Bouwer EJ (2009) Biodegradation and removal of pharmaceuticals and personal care products in treatment systems: a review. Biodegradation 20:441–466.  https://doi.org/10.1007/s10532-008-9237-8 CrossRefPubMedGoogle Scholar
  39. Onesios-Barry KM, Berry D, Proescher JB, Sivakumar IKA, Bouwer EJ (2014) Removal of pharmaceuticals and personal care products during water recycling: microbial community structure and effects of substrate concentration. Appl Environ Microbiol 80:2440–2450.  https://doi.org/10.1128/aem.03693-13 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414.  https://doi.org/10.1111/1462-2920.13023 CrossRefPubMedGoogle Scholar
  41. Park J, Yamashita N, Park C, Shimono T, Takeuchi DM, Tanaka H (2017) Removal characteristics of pharmaceuticals and personal care products: comparison between membrane bioreactor and various biological treatment processes. Chemosphere 179:347–358.  https://doi.org/10.1016/j.chemosphere.2017.03.135 CrossRefPubMedGoogle Scholar
  42. Pino-Otin MR, Muniz S, Val J, Navarro E (2017) Effects of 18 pharmaceuticals on the physiological diversity of edaphic microorganisms. Sci Total Environ 595:441–450.  https://doi.org/10.1016/j.scitotenv.2017.04.002 CrossRefPubMedGoogle Scholar
  43. Pinyakong O et al (2000) Identification of novel metabolites in the degradation of phenanthrene by Sphingomonas sp. strain P2. FEMS Microbiol Lett 191:115–121.  https://doi.org/10.1016/s0378-1097(00)00380-3 CrossRefPubMedGoogle Scholar
  44. Poirier-Larabie S, Segura PA, Gagnon C (2016) Degradation of the pharmaceuticals diclofenac and sulfamethoxazole and their transformation products under controlled environmental conditions. Sci Total Environ 557:257–267.  https://doi.org/10.1016/j.scitotenv.2016.03.057 CrossRefPubMedGoogle Scholar
  45. Pomati F, Castiglioni S, Zuccato E, Fanelli R, Vigetti D, Rossetti C, Calamari D (2006) Effects of a complex mixture of therapeutic drugs at environmental levels on human embryonic cells. Environ Sci Technol 40:2442–2447.  https://doi.org/10.1021/es051715a CrossRefPubMedGoogle Scholar
  46. Pomati F, Orlandi C, Clerici M, Luciani F, Zuccato E (2008) Effects and interactions in an environmentally relevant mixture of pharmaceuticals. Toxicol Sci 102:129–137.  https://doi.org/10.1093/toxsci/kfm291 CrossRefPubMedGoogle Scholar
  47. Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefPubMedGoogle Scholar
  48. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinform 12:18.  https://doi.org/10.1186/1471-2105-12-38 CrossRefGoogle Scholar
  49. Quintana JB, Weiss S, Reemtsma T (2005) Pathway’s and metabolites of microbial degradation of selected acidic pharmaceutical and their occurrence in municipal wastewater treated by a membrane bioreactor. Water Res 39:2654–2664.  https://doi.org/10.1016/j.watres.2005.04.068 CrossRefPubMedGoogle Scholar
  50. Ramos DT, da Silva MLB, Nossa CW, Alvarez PJJ, Corseuil HX (2014) Assessment of microbial communities associated with fermentative-methanogenic biodegradation of aromatic hydrocarbons in groundwater contaminated with a biodiesel blend (B20). Biodegradation 25:681–691.  https://doi.org/10.1007/s10532-014-9691-4 CrossRefPubMedGoogle Scholar
  51. Rauch-Williams T, Hoppe-Jones C, Drewes JE (2010) The role of organic matter in the removal of emerging trace organic chemicals during managed aquifer recharge. Water Res 44:449–460.  https://doi.org/10.1016/j.watres.2009.08.027 CrossRefPubMedGoogle Scholar
  52. Reich-Slotky R et al (2009) Gemfibrozil inhibits Legionella pneumophila and Mycobacterium tuberculosis enoyl coenzyme A reductases and blocks intracellular growth of these bacteria in macrophages. J Bacteriol 191:5262–5271.  https://doi.org/10.1128/jb.00175-09 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rosenberg E (2014) The family Chitinophagaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer, Berlin, pp 493–495Google Scholar
  54. Salveson A, Rauch-Williams T, Dickenson E, Drewes JE, Drury D, McAvoy D, Snyder S (2012) Trace organic compound indicator removal during conventional wastewater treatment. WERF Report CEC4R08Google Scholar
  55. Sathyamoorthy S, Chandran K, Ramsburg CA (2013) Biodegradation and cometabolic modeling of selected beta blockers during ammonia oxidation. Environ Sci Technol 47:12835–12843.  https://doi.org/10.1021/es402878e CrossRefPubMedGoogle Scholar
  56. Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/aem.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Serrano D, Suarez S, Lema JM, Omil F (2011) Removal of persistent pharmaceutical micropollutants from sewage by addition of PAC in a sequential membrane bioreactor. Water Res 45:5323–5333.  https://doi.org/10.1016/j.watres.2011.07.037 CrossRefPubMedGoogle Scholar
  58. Song M, Luo CL, Jiang LF, Zhang DY, Wang YJ, Zhang G (2015) Identification of benzo a pyrene-metabolizing bacteria in forest soils by using DNA-based stable-isotope probing. Appl Environ Microbiol 81:7368–7376.  https://doi.org/10.1128/aem.01983-15 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Stadler LB, Love NG (2016) Impact of microbial physiology and microbial community structure on pharmaceutical fate driven by dissolved oxygen concentration in nitrifying bioreactors. Water Res 104:189–199.  https://doi.org/10.1016/j.watres.2016.08.001 CrossRefPubMedGoogle Scholar
  60. Stasinakis AS, Petalas AV, Mamais D, Thomaidis NS, Gatidou G, Lekkas TD (2007) Investigation of triclosan fate and toxicity in continuous-flow activated sludge systems. Chemosphere 68:375–381.  https://doi.org/10.1016/j.chemosphere.2007.01.047 CrossRefPubMedGoogle Scholar
  61. Sun BZ, Ko K, Ramsay JA (2011) Biodegradation of 1,4-dioxane by a Flavobacterium. Biodegradation 22:651–659.  https://doi.org/10.1007/s10532-010-9438-9 CrossRefPubMedGoogle Scholar
  62. Surovtseva EG, Ivoilov VS, Belyaev SS (1999) Physiological and biochemical properties of Beijerinckia mobilis 1f Phn(+) capable of degrading polycyclic aromatic hydrocarbons. Microbiology 68:746–750Google Scholar
  63. Szokol J, Rucka L, Simcikova M, Halada P, Nesvera J, Patek M (2014) Induction and carbon catabolite repression of phenol degradation genes in Rhodococcus erythropolis and Rhodococcus jostii. Appl Microbiol Biotechnol 98:8267–8279.  https://doi.org/10.1007/s00253-014-5881-6 CrossRefPubMedGoogle Scholar
  64. Takahashi S, Obana Y, Okada S, Abe K, Kera Y (2012) Complete detoxification of tris(1,3-dichloro-2-propyl) phosphate by mixed two bacteria, Sphingobium sp. strain TCM1 and Arthrobacter sp. strain PY1. J Biosci Bioeng 113:79–83.  https://doi.org/10.1016/j.jbiosc.2011.08.020 CrossRefPubMedGoogle Scholar
  65. Tan DT, Arnold WA, Novak PJ (2013) Impact of organic carbon on the biodegradation of estrone in mixed culture systems. Environ Sci Technol 47:12359–12365.  https://doi.org/10.1021/es4027908 CrossRefPubMedGoogle Scholar
  66. Tan DT, Temme HR, Arnold WA, Novak PJ (2015) Estrone degradation: does organic matter (quality), matter? Environ Sci Technol 49:498–503.  https://doi.org/10.1021/es504424v CrossRefPubMedGoogle Scholar
  67. Trinh T, van den Akker B, Stuetz RM, Coleman HM, Le-Clech P, Khan SJ (2012) Removal of trace organic chemical contaminants by a membrane bioreactor. Water Sci Technol 66:1856–1863.  https://doi.org/10.2166/wst.2012.374 CrossRefPubMedGoogle Scholar
  68. Trinh T, van den Akker B, Coleman HM, Stuetz RM, Drewes JE, Le-Clech P, Khan SJ (2016) Seasonal variations in fate and removal of trace organic chemical contaminants while operating a full-scale membrane bioreactor. Sci Total Environ 550:176–183.  https://doi.org/10.1016/j.scitotenv.2015.12.083 CrossRefPubMedGoogle Scholar
  69. Trussell S, Tiwari S, Gerringer F, Trussell R (2015) Enhancing the soil aquifer treatment process for potable reuse. WateReuse Research Foundation. Project 12-12Google Scholar
  70. Wang H, Xie C, Zhu P, Zhou N-Y, Lu Z (2017) Two novel sets of genes essential for nicotine degradation by Sphingomonas melonis TY. Front Microbiol.  https://doi.org/10.3389/fmicb.2016.02060 Google Scholar
  71. Wu XQ, Ernst F, Conkle JL, Gan J (2013) Comparative uptake and translocation of pharmaceutical and personal care products (PPCPs) by common vegetables. Environ Int 60:15–22.  https://doi.org/10.1016/j.envint.2013.07.015 CrossRefPubMedGoogle Scholar
  72. Xun L, Orser CS (1991) Biodegradation of triiodophenol by cell-free extracts of a pentachlorophenol-degrading Flavobacterium sp. Biochem Biophys Res Commun 174:43–48.  https://doi.org/10.1016/0006-291x(91)90482-m CrossRefPubMedGoogle Scholar
  73. Yao L et al (2016) A tetrahydrofolate-dependent methyltransferase catalyzing the demethylation of dicamba in Sphingomonas sp. strain Ndbn-20. Appl Environ Microbiol 82:5621–5630.  https://doi.org/10.1128/aem.01201-16 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Ying GG, Yu XY, Kookana RS (2007) Biological degradation of triclocarban and triclosan in a soil under aerobic and anaerobic conditions and comparison with environmental fate modelling. Environ Pollut 150:300–305.  https://doi.org/10.1016/j.envpol.2007.02.013 CrossRefPubMedGoogle Scholar
  75. Yoon MK, Drewes JE, Amy GL (2013) Fate of bulk and trace organics during a simulated aquifer recharge and recovery (ARR)-ozone hybrid process. Chemosphere 93:2055–2062.  https://doi.org/10.1016/j.chemosphere.2013.07.038 CrossRefPubMedGoogle Scholar
  76. Yu JT, Bouwer EJ, Coelhan M (2006) Occurrence and biodegradability studies of selected pharmaceuticals and personal care products in sewage effluent. Agric Water Manag 86:72–80.  https://doi.org/10.1016/j.agwat.2006.06.015 CrossRefGoogle Scholar
  77. Yu JT, Bisceglia KJ, Bouwer EJ, Roberts AL, Coelhan M (2012) Determination of pharmaceuticals and antiseptics in water by solid-phase extraction and gas chromatography/mass spectrometry: analysis via pentafluorobenzylation and stable isotope dilution. Anal Bioanal Chem 403:583–591.  https://doi.org/10.1007/s00216-012-5846-5 CrossRefPubMedGoogle Scholar
  78. Zhang DQ, Tan SK, Gersberg RM, Sadreddini S, Zhu JF, Nguyen AT (2011a) Removal of pharmaceutical compounds in tropical constructed wetlands. Ecol Eng 37:460–464.  https://doi.org/10.1016/j.ecoleng.2010.11.002 CrossRefGoogle Scholar
  79. Zhang SY, Wang QF, Wan R, Xie SG (2011b) Changes in bacterial community of anthracene bioremediation in municipal solid waste composting soil. J Zhejiang Univ-Sci B 12:760–768.  https://doi.org/10.1631/jzus.B1000440 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Zhang Y, Lv T, Carvalho PN, Arias CA, Chen ZH, Brix H (2016) Removal of the pharmaceuticals ibuprofen and iohexol by four wetland plant species in hydroponic culture: plant uptake and microbial degradation. Environ Sci Pollut Res 23:2890–2898.  https://doi.org/10.1007/s11356-015-5552-x CrossRefGoogle Scholar
  81. Zhou NA, Gough HL (2016) Enhanced biological trace organic contaminant removal: a lab-scale demonstration with bisphenol A-degrading bacteria Sphingobium sp. BiD32. Environ Sci Technol 50:8057–8066.  https://doi.org/10.1021/acs.est.6b00727 CrossRefPubMedGoogle Scholar
  82. Zhou NA, Lutovsky AC, Andaker GL, Gough HL, Ferguson JF (2013) Cultivation and characterization of bacterial isolates capable of degrading pharmaceutical and personal care products for improved removal in activated sludge wastewater treatment. Biodegradation 24:813–827.  https://doi.org/10.1007/s10532-013-9630-9 CrossRefPubMedGoogle Scholar
  83. Zhou NA, Kjeldal H, Gough HL, Nielsen JL (2015) Identification of putative genes involved in bisphenol A degradation using differential protein abundance analysis of Sphingobium sp. BiD32. Environ Sci Technol 49:12232–12241.  https://doi.org/10.1021/acs.est.5b02987 CrossRefPubMedGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Civil and Environmental EngineeringColorado State UniversityFort CollinsUSA
  2. 2.Proteomics and Metabolomics FacilityColorado State UniversityFort CollinsUSA
  3. 3.Division of Pulmonary Sciences and Critical Care MedicineUniversity of Colorado DenverAuroraUSA
  4. 4.Department of Civil and Environmental EngineeringPusan National UniversityBusanRepublic of Korea

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