Abstract
Land application accounts for approximately 50% of wastewater solids disposal in the USA. Yet, little is known regarding the ecological impacts of many non-regulated chemicals found in biosolids. In most previous studies aimed at assessing ecological impacts, a model biosolid is generated by spiking high concentrations of the target chemical into a soil or biosolid. This approach does not account for the interaction of the chemical of interest with the solids throughout the biosolids production process (a.k.a., aging) which may impact the bioavailability and, thus, ultimate toxicity of the chemical. In the present study, using a lab-scale wastewater and digestion treatment system, we generated biosolids which contained aged triclosan and compared ecological impacts to that of spiked biosolids. Ecotoxicity was assessed based on functional and community structure changes to soil denitrifiers, microorganisms critical to nitrogen cycling. A decrease in denitrifier abundance and diversity was observed in the aged biosolids at concentrations of 17.9 ± 1.93 μg/kg while decreases in activity were observed at 26.9 ± 4.6 μg/kg. In the spiked biosolids treatment, lower denitrifier abundance, diversity, and activity were observed at triclosan (TCS) concentrations of 68.6 ± 26.9 μg/kg. This difference suggests a need to better understand TCS bioavailability dynamics.
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References
Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environmental Science & Technology 34(20):4259–4265. https://doi.org/10.1021/es001069+
Alito CL, Gunsch CK (2014) Assessing the effects of silver nanoparticles on biological nutrient removal in bench-scale activated sludge sequencing batch reactors. Environmental Science & Technology 48(2):970–976. https://doi.org/10.1021/es403640j
American Public Health, A., A. D. Eaton, A. American Water Works and F. Water Environment (2005) Standard methods for the examination of water and wastewater. APHA-AWWA-WEF, Washington, D.C.
Anger CT, Sueper C, Blumentrit DJ, McNeill K, Engstrom DR, Arnold WA (2013) Quantification of triclosan, chlorinated triclosan derivatives, and their dioxin photoproducts in lacustrine sediment cores. Environmental Science & Technology 47(4):1833–1843. https://doi.org/10.1021/es3045289
Bailey AM, Constantinidou C, Ivens A, Garvey MI, Webber MA, Coldham N, Hobman JL, Wain J, Woodward MJ, Piddock LJV (2009) Exposure of Escherichia coli and Salmonella enterica serovar Typhimurium to triclosan induces a species-specific response, including drug detoxification. J Antimicrob Chemother 64(5):973–985. https://doi.org/10.1093/jac/dkp320
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541–555. https://doi.org/10.1016/j.mimet.2003.08.009
Bedoux G, Roig B, Thomas O, Dupont V, Le Bot B (2012) Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ Sci Pollut Res 19(4):1044–1065. https://doi.org/10.1007/s11356-011-0632-z
Braker G, Ayala-del-Rio HL, Devol AH, Fesefeldt A, Tiedje JM (2001) Community structure of denitrifiers, Bacteria, and Archaea along redox gradients in pacific northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl Environ Microbiol 67(4):1893–1901. https://doi.org/10.1128/AEM.67.4.1893-1901.2001
Bremer C, Braker G, Matthies D, Reuter A, Engels C, Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-type denitrifier communities in soil. Appl Environ Microbiol 73(21):6876–6884. https://doi.org/10.1128/AEM.01536-07
Butler E, Whelan MJ, Ritz K, Sakrabani R, van Egmond R (2011) Effects of triclosan on soil microbial respiration. Environ Toxicol Chem 30(2):360–366. https://doi.org/10.1002/etc.405
Chalew TEA, Halden RU (2009) Environmental exposure of aquatic and terrestrial biota to triclosan and triclocarban. JAWRA Journal of the American Water Resources Association 45(1):4–13. https://doi.org/10.1111/j.1752-1688.2008.00284.x
Chariton AA, Ho KT, Proestou D, Bik H, Simpson SL, Portis LM, Cantwell MG, Baguley JG, Burgess RM, Pelletier MM (2014) A molecular-based approach for examining responses of eukaryotes in microcosms to contaminant-spiked estuarine sediments. Environ Toxicol Chem 33(2):359–369. https://doi.org/10.1002/etc.2450
Consortium T (2002) High production volume (HPV) chemical challenge program data availability and screening level assessment for triclocarban: CAS #: 101-20-2. U. E. P, Agency
Davis EF, Gunsch CK, Stapleton HM (2015) Fate of flame retardants and the antimicrobial agent triclosan in planted and unplanted biosolid-amended soils. Environ Toxicol Chem 34(5):968–976. https://doi.org/10.1002/etc.2854
Davis EF, Klosterhaus SL, Stapleton HM (2012) Measurement of flame retardants and triclosan in municipal sewage sludge and biosolids. Environ Int 40:1–7. https://doi.org/10.1016/j.envint.2011.11.008
Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71(12):8335–8343. https://doi.org/10.1128/AEM.71.12.8335-8343.2005
Farré M, Asperger D, Kantiani L, González S, Petrovic M, Barceló D (2008) Assessment of the acute toxicity of triclosan and methyl triclosan in wastewater based on the bioluminescence inhibition of Vibrio fischeri. Anal Bioanal Chem 390(8):1999–2007. https://doi.org/10.1007/s00216-007-1779-9
Graham DW, Trippett C, Dodds WK, O’Brien JM, Banner EBK, Head IM, Smith MS, Yang RK, Knapp CW (2010) Correlations between in situ denitrification activity and nir-gene abundances in pristine and impacted prairie streams. Environ Pollut 158(10):3225–3229. https://doi.org/10.1016/j.envpol.2010.07.010
Green TGJ, Mueller JP, Chamblee DS (n.d.) Planting guide for forage crops in North Carolina. North Carolina State University, Raleigh, North Carolina
Groffman P, Holland E, Myrold D, Robertson G, Zou X (1999) Standard soil methods for long-term ecological research. Oxford University Press, Oxford
Grove C, Liebenberg W, Du Preez JL, Yang WZ, De Villiers MM (2003) Improving the aqueous solubility of triclosan by solubilization, complexation, and in situ salt formation. J Cosmet Sci 54(6):537–550
Hardy DH, T. M., Stokes CE (2014). Crop fertilization based on North Carolina soil tests. A. D. Department of Agriculture and Consumer Services. North Caroliner. Circular No. 1
Harrison EZ, Oakes SR, Hysell M, Hay A (2006) Organic chemicals in sewage sludges. Sci Total Environ 367(2–3):481–497. https://doi.org/10.1016/j.scitotenv.2006.04.002
Harrow DI, Felker JM and Baker KH (2011). Impacts of triclosan in greywater on soil microorganisms. Appl Environ Soil Sci
Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59(3):327–335. https://doi.org/10.1016/j.mimet.2004.07.002
Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72(8):5181–5189. https://doi.org/10.1128/AEM.00231-06
Ho KT, Chariton AA, Portis LM, Proestou D, Cantwell MG, Baguley JG, Burgess RM, Simpson S, Pelletier MC, Perron MM (2013) Use of a novel sediment exposure to determine the effects of triclosan on estuarine benthic communities. Environ Toxicol Chem 32(2):384–392. https://doi.org/10.1002/etc.2067
Holzem R, Gardner C and Gunsch C (2017) Evaluating the impacts of triclosan on wastewater treatment performance during startup and acclimation. Water Sci Technol: wst2017566
Holzem RM, Stapleton HM and Gunsch CK (2014). Determining the ecological impacts of organic contaminants in biosolids using a high-throughput colorimetric denitrification assay: a case study with antimicrobial agents. Environmental Science & Technology
Ikuma K, Holzem RM, Gunsch CK (2012) Impacts of organic carbon availability and recipient bacteria characteristics on the potential for TOL plasmid genetic bioaugmentation in soil slurries. Chemosphere 89(2):158–163. https://doi.org/10.1016/j.chemosphere.2012.05.086
Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72(9):5957–5962. https://doi.org/10.1128/AEM.00439-06
Kinney CA, Furlong ET, Kolpin DW, Burkhardt MR, Zaugg SD, Werner SL, Bossio JP, Benotti MJ (2008) Bioaccumulation of pharmaceuticals and other anthropogenic waste indicators in earthworms from agricultural soil amended with biosolid or swine manure. Environmental Science & Technology 42(6):1863–1870. https://doi.org/10.1021/es702304c
Kinney CA, Furlong ET, Zaugg SD, Burkhardt MR, Werner SL, Cahill JD, Jorgensen GR (2006) Survey of organic wastewater contaminants in biosolids destined for land application. Environmental Science & Technology 40(23):7207–7215. https://doi.org/10.1021/es0603406
Levy CW, Roujeinikova A, Sedelnikova S, Baker PJ, Stuitje AR, Slabas AR, Rice DW, Rafferty JB (1999) Molecular basis of triclosan activity. Nature 398(6726):383–384. https://doi.org/10.1038/18803
Liu F, Ying G-G, Yang L-H, Zhou Q-X (2009) Terrestrial ecotoxicological effects of the antimicrobial agent triclosan. Ecotoxicol Environ Saf 72(1):86–92. https://doi.org/10.1016/j.ecoenv.2008.06.009
Lozano N, Rice CP, Ramirez M, Torrents A (2010) Fate of triclosan in agricultural soils after biosolid applications. Chemosphere 78(6):760–766. https://doi.org/10.1016/j.chemosphere.2009.10.043
Lukow T, Dunfield PF, Liesack W (2000) Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol Ecol 32(3):241–247. https://doi.org/10.1111/j.1574-6941.2000.tb00717.x
Macherius A, Eggen T, Lorenz WG, Reemtsma T, Winkler U, Moeder M (2012) Uptake of galaxolide, tonalide, and triclosan by carrot, barley, and meadow fescue plants. J Agric Food Chem 60(32):7785–7791. https://doi.org/10.1021/jf301917q
McClellan K, Halden RU (2010) Pharmaceuticals and personal care products in archived US biosolids from the 2001 EPA national sewage sludge survey. Water Res 44(2):658–668. https://doi.org/10.1016/j.watres.2009.12.032
McMurry LM, Oethinger M, Levy SB (1998) Triclosan targets lipid synthesis. Nature 394(6693):531–532. https://doi.org/10.1038/28970
McNamara PJ, Krzmarzick MJ (2013) Triclosan enriches for Dehalococcoides-like Chloroflexi in anaerobic soil at environmentally relevant concentrations. FEMS Microbiol Lett 344(1):48–52. https://doi.org/10.1111/1574-6968.12153
McNamara PJ, LaPara TM, Novak PJ (2014) The impacts of triclosan on anaerobic community structures, function, and antimicrobial resistance. Environmental Science & Technology 48(13):7393–7400. https://doi.org/10.1021/es501388v
McNamara PJ, Levy SB (2016) Triclosan: an instructive tale. Antimicrob Agents Chemother 60(12):7015–7016. https://doi.org/10.1128/AAC.02105-16
Neumegen RA, Fernandez-Alba AR, Chisti Y (2005) Toxicities of triclosan, phenol, and copper sulfate in activated sludge. Environ Toxicol 20(2):160–164. https://doi.org/10.1002/tox.20090
Pannu MW, O'Connor GA, Toor GS (2012) Toxicity and bioaccumulation of biosolids-borne triclosan in terrestrial organisms. Environ Toxicol Chem 31(3):646–653. https://doi.org/10.1002/etc.1721
Park I, Zhang N, Ogunyoku TA, Young TM, Scow KM (2013) Effects of triclosan and biosolids on microbial community composition in an agricultural soil. Water Environment Research 85(12):2237–2242. https://doi.org/10.2175/106143012X13560205144335
Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96(96):249–305. https://doi.org/10.1016/S0065-2113(07)96003-4
Philippot L, Piutti S, Martin-Laurent F, Hallet S, Germon JC (2002) Molecular analysis of the nitrate-reducing community from unplanted and maize-planted soils. Appl Environ Microbiol 68(12):6121–6128. https://doi.org/10.1128/AEM.68.12.6121-6128.2002
Reiss R, Lewis G, Griffin J (2009) An ecological risk assessment for triclosan in the terrestrial environment. Environ Toxicol Chem 28(7):1546–1556. https://doi.org/10.1897/08-250.1
Rooklidge SJ (2004) Environmental antimicrobial contamination from terraccumulation and diffuse pollution pathways. Sci Total Environ 325(1–3):1–13. https://doi.org/10.1016/j.scitotenv.2003.11.007
Rosenberg S (2000) Consumer and market use of antibacterials at home. Pediatr Infect Dis J 19(10):S114–S116. https://doi.org/10.1097/00006454-200010001-00006
Scala DJ, Kerkhof LJ (2000) Horizontal heterogeneity of denitrifying bacterial communities in marine sediments by terminal restriction fragment length polymorphism analysis. Appl Environ Microbiol 66(5):1980–1986. https://doi.org/10.1128/AEM.66.5.1980-1986.2000
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(2):375–381. https://doi.org/10.1016/j.chemosphere.2007.01.047
Tiedje JM, Firestone RB, Firestone MK, Betlach MR, Smith MS, Caskey WH (1979) Methods for the production and use of nitrogen-13 in studies of denitrification. Soil Sci Soc Am J 43(4):709–716. https://doi.org/10.2136/sssaj1979.03615995004300040016x
Topp E, Monteiro SC, Beck A, Coelho BB, Boxall ABA, Duenk PW, Kleywegt S, Lapen DR, Payne M, Sabourin L, Li H, Metcalfe CD (2008) Runoff of pharmaceuticals and personal care products following application of biosolids to an agricultural field. Sci Total Environ 396(1):52–59. https://doi.org/10.1016/j.scitotenv.2008.02.011
USEPA (2009) Targeted national sewge sludge survey sampling and analysis technical report. U. E. P. A. O. o. Water, Washington DC
Větrovský T, Baldrian P (2013) The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One 8(2):e57923. https://doi.org/10.1371/journal.pone.0057923
Waller NJ, Kookana RS (2009) Effect of triclosan on microbial activity in australian soils. Environ Toxicol Chem 28(1):65–70. https://doi.org/10.1897/08-224.1
Wang S, Gunsch CK (2011) Effects of selected pharmaceutically active compounds on treatment performance in sequencing batch reactors mimicking wastewater treatment plants operations. Water Res 45(11):3398–3406. https://doi.org/10.1016/j.watres.2011.03.055
Wilderer PA, Jones WL, Dau U (1987) Competition in denitrification systems affecting reduction rate and accumulation of nitrite. Water Res 21(2):239–245. https://doi.org/10.1016/0043-1354(87)90056-X
Wolsing M, Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48(2):261–271. https://doi.org/10.1016/j.femsec.2004.02.002
Wu C, Spongberg AL, Witter JD, Fang M, Czajkowski KP (2010) Uptake of pharmaceutical and personal care products by soybean plants from soils applied with biosolids and irrigated with contaminated water. Environmental Science & Technology 44(16):6157–6161. https://doi.org/10.1021/es1011115
Ying G-G, Kookana RS (2007) Triclosan in wastewaters and biosolids from Australian wastewater treatment plants. Environ Int 33(2):199–205. https://doi.org/10.1016/j.envint.2006.09.008
Zaayman M, Siggins A, Horne D, Lowe H, Horswell J (2017) Investigation of triclosan contamination on microbial biomass and other soil health indicators. FEMS Microbiol Lett 364(16). https://doi.org/10.1093/femsle/fnx163
Zumft W (1999) The denitrifying prokaryotes. The prokaryotes: an evolving electronic resource for the microbiologial community. S. f. M. Dworkin, E. Rosenberg, K.-H Schelider, and E. Stackebrandt
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533–616
Acknowledgements
This work was supported by the National Science Foundation (NSF) under grant no. CBET 0854167. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of NSF. We thank Dr. Heather Stapleton’s lab at Duke University, particularly Dr. Elizabeth Davis and Thomas (Mingliang Fang) for providing the analytical support. We also thank Dr. Emily Bernhardt’s lab at Duke University, particularly Brooke Hassett for providing help with the DEA assay.
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Highlights
• This study assessed the impact of biosolids aging on denitrification.
• Aged biosolids treatments were affected at lower triclosan levels than spiked treatments.
• This work suggests a need to better understand triclosan bioavailability dynamics.
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Holzem, R.M., Gardner, C.M., Stapleton, H.M. et al. Using laboratory-generated biosolids to evaluate the microbial ecotoxicity of triclosan in a simulated land application scenario. Environ Sci Pollut Res 25, 11084–11099 (2018). https://doi.org/10.1007/s11356-017-1147-z
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DOI: https://doi.org/10.1007/s11356-017-1147-z