Abstract
Pharmaceutical and personal care products (PPCPs) discharged with wastewater treatment plant (WWTP) effluents are an emerging surface water quality concern. Biological transformation has been identified as an important removal mechanism during wastewater treatment. The aim of this research was the identification of bacteria with characteristics for potential bioaugmentation to enhance PPCP removal. We report here the cultivation and characterization of bacteria capable of degrading PPCPs to ng/L concentrations. An isolation approach was developed using serial enrichment in mineral medium containing 1 mg/L of an individual PPCP as the sole organic carbon source available to heterotrophs until the original activated sludge inocula was diluted to ~10−8 of its initial concentration, followed by colony growth on solid R2A agar. Eleven bacteria were isolated, eight that could remove triclosan, bisphenol A, ibuprofen, or 17β-estradiol to below 10 ng/L, one that could remove gemfibrozil to below 60 ng/L, and two that could remove triclosan or E2, but not to ng/L concentrations. Most bacterial isolates degraded contaminants during early growth when grown utilizing rich carbon sources and were only able to degrade the PPCPs on which they were isolated. Seven of the bacterial isolates were sphingomonads, including all the triclosan and bisphenol A degraders and the ibuprofen degrader. The study results indicate that the isolated bacteria may have a positive influence on removal in WWTPs if present at sufficient concentrations and may be useful for bioaugmentation.
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Anari MR, Bakhtiar R, Zhu B, Huskey S, Franklin RB, Evans DC (2002) Derivatization of ethinylestradiol with dansyl chloride to enhance electrospray ionization: application in trace analysis of ethinylestradiol in rhesus monkey plasma. Anal Chem 74:4136–4144. doi:10.1021/ac025712h
Andersen H, Siegrist H, Halling-Sorensen B, Ternes TA (2003) Fate of estrogens in a municipal sewage treatment plant. Environ Sci Technol 37:4021–4026. doi:10.1021/es026192a
AWWA (1998) Standard methods for the examination of water and wastewater. American Water Works Association, New York
Ballesteros-Gomez A, Ruiz F, Rubio S, Perez-Bendito D (2007) Determination of bisphenols A and F and their diglycidyl ethers in wastewater and river water by coacervative extraction and liquid chromatography-fluorimetry. Anal Chim Acta 603:51–59. doi:10.1016/j.aca.2007.09.048
Bester K (2003) Triclosan in a sewage treatment process: balances and monitoring data. Water Res 37:3891–3896. doi:10.1016/S0043-1354(03)00335-X
Brausch JM, Rand GM (2011) A review of personal care products in the aquatic environment: environmental concentrations and toxicity. Chemosphere 82:1518–1532. doi:10.1016/j.chemosphere.2010.11.018
Burkhardt-Holm P, Segner H, Burki R, Peter A, Schubert S, Suter MJF, Borsuk ME (2008) Estrogenic endocrine disruption in Switzerland: assessment of fish exposure and effects. Chimia 62:376–382. doi:10.2533/chimia.2008.376
Carballa M, Omil F, Lema JM, Llompart M, Garcia-Jares C, Rodriguez I, Gomez M, Ternes T (2004) Behavior of pharmaceuticals, cosmetics and hormones in a sewage treatment plant. Water Res 38:2918–2926. doi:10.1016/j.watres.2004.03.029
Chimchirian RF, Suri RPS, Fu H (2007) Free synthetic and natural estrogen hormones in influent and effluent of three municipal wastewater treatment plants. Water Environ Res 79:969–974. doi:10.2175/106143007X175843
Coogan MA, Edziyie RE, La Point TW, Venables BJ (2007) Algal bioaccumulation of triclocarban, triclosan, and methyl-triclosan in a North Texas wastewater, treatment plant receiving stream. Chemosphere 67:1911–1918. doi:10.1016/j.chemosphere.2006.12.027
Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107:907–938. doi:10.2307/3434573
Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689. doi:10.1073/pnas.89.12.5685
Dickenson ERV, Snyder SA, Sedlak DL, Drewes JE (2011) Indicator compounds for assessment of wastewater effluent contributions to flow and water quality. Water Res 45:1199–1212. doi:10.1016/j.watres.2010.11.012
Duong CN, Ra JS, Cho J, Kim SD, Choi HK, Park J, Kim KW, Inam E, Kim SD (2010) Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78:286–293. doi:10.1016/j.chemosphere.2009.10.048
Fair PA, Lee H, Adams J, Darling C, Pacepavicius G, Alaee M, Bossart GD, Henry N, Muir D (2009) Occurrence of triclosan in plasma of wild Atlantic bottlenose dolphins (Tursiops truncatus) and in their environment. Environ Pollut 157:2248–2254. doi:10.1016/j.envpol.2009.04.002
Federle TW, Kaiser SK, Nuck BA (2002) Fate and effects of triclosan in activated sludge. Environ Toxicol Chem 21:1330–1337. doi:10.1897/1551-5028(2002)021<1330:FAEOTI>2.0.CO;2
Fraker SL, Smith GR (2004) Direct and interactive effects of ecologically relevant concentrations of organic wastewater contaminants on Rana pipiens tadpoles. Environ Toxicol 19:250–256. doi:10.1002/tox.20017
Froehner S, Piccioni W, Machado KS, Aisse MM (2011) Removal capacity of caffeine, hormones, and bisphenol by aerobic and anaerobic sewage treatment. Water Air Soil Pollut 216:463–471. doi:10.1007/s11270-010-0545-3
Frothingham R, Allen RL, Wilson KH (1991) Rapid 16S ribosomal DNA sequencing from a single colony without DNA extraction or purification. Biotechniques 11:40–44
Fry NK, Fredrickson JK, Fishbain S, Wagner M, Stahl DA (1997) Population structure of microbial communities associated with two deep, anaerobic, alkaline aquifers. Appl Environ Microbiol 63:1498–1504
Gross B, Montgomery-Brown J, Naumann A, Reinhard M (2004) Occurrence and fate of pharmaceuticals and alkylphenol ethoxylate metabolites in an effluent-dominated river and wetland. Environ Toxicol Chem 23:2074–2083. doi:10.1897/03-606
Hay AG, Dees PM, Sayler GS (2001) Growth of a bacterial consortium on triclosan. FEMS Microbiol Ecol 36:105–112. doi:10.1111/j.1574-6941.2001.tb00830.x
Heidler J, Halden RU (2007) Mass balance assessment of triclosan removal during conventional sewage treatment. Chemosphere 66:362–369. doi:10.1016/j.chemosphere.2006.04.066
Joss A, Andersen J, Ternes T, Richle PR, Siegrist H (2004) Removal of estrogens in municipal wastewater treatment under aerobic and anaerobic conditions: consequences for plant optimization. Environ Sci Technol 38:3047–3055. doi:10.1021/es0351488
Kim Y, Murugesan K, Schmidt S, Bokare V, Jeon J, Kim E, Chang Y (2011) Triclosan susceptibility and co-metabolism: A comparison for three aerobic pollutant-degrading bacteria. Bioresour Technol 102:2206–2212. doi:10.1016/j.biortech.2010.10.009
Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211. doi:10.1021/es011055j
Kurisu F, Ogura M, Saitoh S, Yamazoe A, Yagi O (2010) Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp and Sphingomonas sp. J Biosci Bioeng 109:576–582. doi:10.1016/j.jbiosc.2009.11.006
Layton AC, Gregory BW, Seward JR, Schultz TW, Sayler GS (2000) Mineralization of steroidal hormones by biosolids in wastewater treatment systems in Tennessee USA. Environ Sci Technol 34:3925–3931. doi:10.1021/es9914487
Li G, Zu L, Wong P, Hui X, Lu Y, Xiong J, An T (2012a) Biodegradation and detoxification of bisphenol A with one newly-isolated strain Bacillus sp GZB: kinetics, mechanism and estrogenic transition. Bioresour Technol 114:224–230. doi:10.1016/j.biortech.2012.03.067
Li Z, Nandakumar R, Madayiputhiya N, Li X (2012b) Proteomic analysis of 17β-estradiol degradation by Stenotrophomonas maltophilia. Environ Sci Technol 46:5947–5955. doi:10.1021/es300273k
Lin AYC, Reinhard M (2005) Photodegradation of common environmental pharmaceuticals and estrogens in river water. Environ Toxicol Chem 24:1303–1309. doi:10.1897/04-236R.1
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi:10.1093/nar/gkh293
Meade MJ, Waddell RL, Callahan TM (2001) Soil bacteria Pseudomonas putida and Alcaligenes xylosoxidans subsp denitrificans inactivate triclosan in liquid and solid substrates. FEMS Microbiol Lett 204:45–48. doi:10.1111/j.1574-6968.2001.tb10860.x
Metcalfe CD, Metcalfe TL, Kiparissis Y, Koenig BG, Khan C, Hughes BJ, Croley TR, March RE, Potter T (2001) Estrogenic potency of chemicals detected in sewage treatment plant effluents as determined by in vivo assays with Japanese medaka (Oryzias latipes). Environ Toxicol Chem 20:297–308. doi:10.1897/1551-5028(2001)020<0297:EPOCDI>2.0.CO;2
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. doi:10.1128/AEM.71.10.6121-6125.2005
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. doi:10.1007/s10532-008-9237-8
Oshiman K, Tsutsumi Y, Nishida T, Matsumura Y (2007) Isolation and characterization of a novel bacterium, Sphingomonas bisphenolicum strain AO1, that degrades bisphenol A. Biodegradation 18:247–255. doi:10.1007/s10532-006-9059-5
Pauwels B, Wille K, Noppe H, De Brabander H, van de Wiele T, Verstraete W, Boon N (2008) 17alpha-ethinylestradiol cometabolism by bacteria degrading estrone, 17beta-estradiol and estriol. Biodegradation 19:683–693. doi:10.1007/s10532-007-9173-z
Paxeus N (2004) Removal of selected non-steroidal anti-inflammatory drugs (NSAIDs), gemfibrozil, carbamazepine, beta-blockers, trimethoprim and triclosan in conventional wastewater treatment plants in five EU countries and their discharge to the aquatic environment. Water Sci Technol 50:253–260
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. doi:10.1016/j.watres.2005.04.068
Reasoner DJ, Geldreich EE (1979) A new medium for the enumeration and sub culture of bacteria from potable water. Abstracts of the annual meeting of the American Society for Microbiology 79:180
Sakai K, Yamanaka H, Moriyoshi K, Ohmoto T, Ohe T (2007) Biodegradation of bisphenol A and related compounds by Sphingomonas sp strain BP-7 isolated from seawater. Biosci Biotechnol Biochem 71:51–57. doi:10.1271/bbb.60351
Santos JL, Aparicio I, Alonso E (2007) Occurrence and risk assessment of pharmaceutically active compounds in wastewater treatment plants. A case study: Seville city (Spain). Environ Int 33:596–601. doi:10.1016/j.envint.2006.09.014
Scheytt T, Mersmann P, Lindstadt R, Heberer T (2005) 1-Octanol/water partition coefficients of 5 pharmaceuticals from human medical care: carbamazepine, clofibric acid, diclofenac, ibuprofen, and propyphenazone. Water Air Soil Pollut 165:3–11. doi:10.1007/s11270-005-3539-9
Stasinakis AS, Gatidou G, Mamais D, Thomaidis NS, Lekkas TD (2008) Occurrence and fate of endocrine disrupters in Greek sewage treatment plants. Water Res 42:1796–1804. doi:10.1016/j.watres.2007.11.003
Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81:793–811. doi:10.1007/s00253-008-1752-3
Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417
Tanner RS (1997) Manual of environmental microbiology. ASM Press, Washington, D.C
Teske A, Sigalevich P, Cohen Y, Muyzer G (1996) Molecular identification of bacteria from a coculture by denaturing gradient gel electrophoresis of 16S ribosomal DNA fragments as a tool for isolation in pure cultures. Appl Environ Microbiol 62:4210–4215
Toyama T, Sato Y, Inoue D, Sei K, Chang Y, Kikuchi S, Ike M (2009) Biodegradation of bisphenol A and bisphenol F in the rhizosphere sediment of Phragmites australis. J Biosci Bioeng 108:147–150. doi:10.1016/j.jbiosc.2009.03.011
US EPA, Office of Research and Development. Basic information, Pharmaceutical and personal care products (PPCPs), US EPA. http://epa.gov/ppcp/basic2.html. Accessed 14 Aug 2012
Westerhoff P, Yoon Y, Snyder S, Wert E (2005) Fate of endocrine-disruptor, pharmaceutical, and personal care product chemicals during simulated drinking water treatment processes. Environ Sci Technol 39:6649–6663. doi:10.1021/es0484799
Wilson BA, Smith VH, Denoyelles F, Larive CK (2003) Effects of three pharmaceutical and personal care products on natural freshwater algal assemblages. Environ Sci Technol 37:1713–1719. doi:10.1021/es0259741
Yang X, Flowers RC, Weinberg HS, Singer PC (2011) Occurrence and removal of pharmaceuticals and personal care products (PPCPs) in an advanced wastewater reclamation plant. Water Res 45:5218–5228. doi:10.1016/j.watres.2011.07.026
Yu JC, Kwong TY, Luo Q, Cai Z (2006) Photocatalytic oxidation of triclosan. Chemosphere 65:390–399. doi:10.1016/j.chemosphere.2006.02.011
Yu C, Roh H, Chu K (2007) 17beta-estradiol-degrading bacteria isolated from activated sludge. Environ Sci Technol 41:486–492. doi:10.1021/es060923f
Zhang C, Zeng G, Yuan L, Yu J, Li J, Huang G, Xi B, Liu H (2007) Aerobic degradation of bisphenol A by Achromobacter xylosoxidans strain B-16 isolated from compost leachate of municipal solid waste. Chemosphere 68:181–190. doi:10.1016/j.chemosphere.2006.12.012
Zhang Z, Feng Y, Gao P, Wang C, Ren N (2011) Occurrence and removal efficiencies of eight EDCs and estrogenicity in a STP. J Environ Monit 13:1366–1373. doi:10.1039/c0em00597e
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Funding was provided by the National Science Foundation (CBET 0829132) and the King County Fellowship Program. We thank Venkateswarlu Nanaboina for his assistance developing LC–MS/MS methods.
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Zhou, N.A., Lutovsky, A.C., Andaker, G.L. et al. 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 (2013). https://doi.org/10.1007/s10532-013-9630-9
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DOI: https://doi.org/10.1007/s10532-013-9630-9