Abstract
Aims
Limited information is available on plant rhizosphere processes for removing antibiotics in antibiotic-contaminated waters. This study identifies rhizosphere processes and evaluates their relative contributions for the macrolides (ML) removal in aquatic plant systems.
Methods
A flask-scale experiment (100 and 300 μg/L ML) incorporating Juncus effuses and Canna indica was used to identify the root adsorption, rhizobacterial influences, and plant uptake responsible for the ML (i.e., anhydroerythromycin A, roxithromycin, clarithromycin and tilmicosin) removal.
Results
Total ML removal rates due to rhizosphere processes were respectively 43.7–67.6% and 44.3–82.2% at 100 and 300 μg/L ML. J. effuses removed ML more effectively than C. indica (P < 0.05). The relative contribution of rhizospheric pathways to remove all ML followed the order: root sorption > rhizobacterial influence > plant uptake (P < 0.01). Sorption and rhizobacterial activity were important removal pathways in wetland plant microcosms, accounting for 36.5–72.8% and 20.5–54.2% of the total rhizosphere associated removal of ML, respectively.
Conclusions
Root sorption and rhizobacterial influence were the main rhizospheric pathways of ML removal in aquatic plant systems. Fe plaque on the root surface, rhizobacterial number and bacterial activity play significant roles in the removal of target pollutants.
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References
Amils R, Fuente D, Rodriguez N, Zuluaga J, Menéndez N, Tornero J (2007) Composition, speciation and distribution of iron minerals in Imperata Cylindrica. Plant Physiol Biochem 45:335–340. doi:10.1016/j.plaphy.2007.03.020
Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–232
Blamey F, Pax C, Wehr JB, Wang P, Menzies NW, Kopittke PM (2014) Kinetics and mechanisms of cowpea root adaptation to changes in solution calcium. Plant Soil 379:301–314. doi:10.1007/s11104-014-2065-1
Brix H, Koottatep T, Laugesen C (2007) Wastewater treatment in tsunami affected areas of Thailand by constructed wetlands. Water Sci Technol 56:69–74. doi:10.2166/wst.2007.528
Burken JG, Schnoor JL (1997) Uptake and metabolism of Atrazine by poplar trees. Environ Sci Technol 31(5):1399–1406
Chehrenegar B, Hu J, Ong SL (2016) Active removal of ibuprofen by money plant enhanced by ferrous ions. Chemosphere 144:91–96. doi:10.1016/j.chemosphere.2015.08.060
Chen C, Dixon J, Turner F (1980) Iron coatings on rice roots: morphology and models of development. Soil Sci Soc Am J 44:1113–1119. doi:10.2136/sssaj1980.03615995004400050046x
Chen Y, Wen Y, Zhou Q, Vymazal J (2014) Effects of plant biomass on nitrogen transformation in subsurface-batch constructed wetlands: a stable isotope and mass balance assessment. Water Res 63:158–167. doi:10.1016/j.watres.2014.06.015
Chen Y, Wen Y, Zhou J, Zhou Q, Vymazal J, Kuschk P (2015) Transformation of chloroform in model treatment wetlands: from mass balance to microbial analysis. Environ Sci Technol 49:6198–6205. doi:10.1021/es506357e
Cheng H, Wang M, Hung MW, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148. doi:10.1007/s11104-013-1945-0
Choo S, Um Y, Han SO, Woo HM (2016) Engineering of Corynebacterium glutamicum to utilize methyl acetate, a potential feedstock derived by carbonylation of methanol with CO. J Biotechnol 224:47–50
Dan A, Yang Y, Dai YN, Chen CX, Wang SY, Tao R (2013) Removal and factors influencing removal of sulfonamides and trimethoprim from domestic sewage in constructed wetlands. Bioresour Technol 146:363–370. doi:10.1016/j.biortech.2013.07.050
Datta R, Das P, Smith SP, Pravin RDM, Reddy R, Sarkar D (2013) Phytoremediation potential of vetiver grass [chrysopogon zizanioides(L.)] for tetracycline. Int J Phytorem 15:343–351. doi:10.1080/15226514.2012.702803
Dettenmaier EM, Doucette WJ, Bugbee B (2009) Chemical hydrophobicity and uptake by plant roots. Environ Sci Technol 43:324–329. doi:10.1021/es801751x
Dietz AC, Schnoor JL (2001) Advances in phytoremediation. Environ Health Perspect 109(Supplement 1):163–168
Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep-UK 7:1–8. doi:10.1038/srep44641
Faulwetter JL, Gagnon V, Sundberg C, Chazarenc F, Burr MD, Brisson J, Camper AK, Stein OR (2009) Microbial processes influencing performance of treatment wetlands: a review. Ecol Eng 35(6):987–1004. doi:10.1016/j.ecoleng.2008.12.030
Feitosa-Felizzola J, Hanna K, Chiron S (2009) Adsorption and transformation of selected human-used macrolide antibacterial agents with iron (III) and manganese (IV) oxides. Environ Pollut 157(4):1317–1322. doi:10.1016/j.envpol.2008.11.048
Gagnon V, Chazarenc F, Brisson J (2012) Effect of plant species on water quality at the outlet of a sludge treatment wetland. Water Res 46(16):5305–5315. doi:10.1016/j.watres.2012.07.007
Gros M, Petrovic M, Barcelo D (2007) Wastewater treatment plants as a pathway for aquatic contamination by pharmaceuticals in the Ebro river basin (Northeast Spain). Environ Toxicol Chem 26:1553–1562. doi:10.1897/06-495R.1
Grujic S, Vasiljevic T, Lausevic M (2009) Determination of multiple pharmaceutical classes in surface and ground waters by liquid chromatography-ion trap-tandem mass spectrometry. J Chromatogr A 1216:4989–5000. doi:10.1016/j.chroma.2009.04.059
Gujarathi NP, Haney BJ, Linden JC (2005) Phytoremediation potential of Myriophyllum Aquaticum and Pista Stratiotes to modify antibiotic growth promoters, tetracycline, oxytetracycline, in aqueous wastewater systems. Int J Phytorem 7:99–112. doi:10.1080/16226510590950405
Hadad HR, Maine MA, Bonetto CA (2006) Macrophyte growth in a pilot-scale constructed wetland for industrial wastewater treatment. Chemosphere 63(10):1744–1753
Hadibarata T, Zubir M, Rubiyatno CT (2013) Microbial transformation and sorption of anthracene in liquid culture. Bioprocess Biosyst Eng 36:1229–1233. doi:10.1007/s00449-012-0850-x
Hamdan I (2003) Comparative in-vitro investigations of the interaction between some macrolides and cu (II), Zn (II) and Fe (II). Pharmazie 58:223–224
Hernando MD, Mezcua M, Fernandez-Albá AR, Barceló D (2006) Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334–342. doi:10.1016/j.talanta.2005.09.037
Hijosa-Valsero M, Fink G, Schlüsener MP, Sidrach-Cardona R, Martín-Villacorta R, Ternes T, Bécares E (2011) Removal of antibiotics from urban wastewater by constructed wetland optimization. Chemosphere 83(5):713–719. doi:10.1016/j.chemosphere.2011.02.004
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. University of California, Berkeley, p 39
Jelić A, Petrović M, Barceló D (2009) Multi-residue method for trace level determination of pharmaceuticals in solid samples using pressurized liquid extraction followed by liquid chromatography/quadrupole-linear ion trap mass spectrometry. Talanta 80:363–371. doi:10.1016/j.talanta.2009.06.077
Konnerup D, Brix H (2010) Nitrogen nutrition of Canna indica: effects of ammonium versus nitrate on growth, biomass allocation, photosynthesis, nitrate reductase activityand N uptake rates. Aquat Bot 92:142–148. doi:10.1016/j.aquabot.2009.11.004
Kumwimba M, Dzakpasu M, Zhu B, Muyembe D (2016) Uptake and release of sequestered nutrient in subtropical monsoon ecological ditch plant species. Water Air Soil Pollut 227:405–418. doi:10.1007/s11270-016-3105-7
LaPara TM, Burch TR, McNamara PJ, Tan DT, Yan M, Eichmiller JJ (2011) Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior Harbor. Environ Sci Technol 45:9543–9549. doi:10.1021/es202775r
Li L, Yang Y, Tam N, Yang L, Mei X, Yang F (2013) Growth characteristics of six wetland plants and their influences on domestic wastewater treatment efficiency. Ecol Eng 60:382–392. doi:10.1016/j.ecoleng.2013.09.044
Liu W, Zhu Y, Hu Y, Williams P, Gault A, Meharg A, Charnock J, Smith F (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza Sativa L.) Environ Sci Technol 40:5730–5736. doi:10.1021/es060800v
Liu F, Ying GG, Tao R, Zhao JL, Yang JF, Zhao LF (2009) Effects of six selected antibiotics on plant growth and oil microbial and enzymatic activities. Environ Pollut 157:1636–1642. doi:10.1016/j.envpol.2008.12.021
Liu L, Liu Y, Liu C, Wang Z, Dong J, Zhu G, Huang X (2013) Potential effect and accumulation of veterinary antibiotics in Phragmites Australis under hydroponic conditions. Ecol Eng 53:138–143. doi:10.1016/j.ecoleng.2012.12.033
Makris KC, Shakya M, Datta R, Sarkar D, Pachanoor D (2007) High uptake of 2,4,6-trinitrotoluene by vetiver grass potential for phytoremediation? Environ Pollut 146:1–4. doi:10.1016/j.envpol.2006.06.020
Managaki S, Murata A, Takada H, Tuyen B, Chiem N (2007) Distribution of macrolides, sulfonamides and trimethoprim in tropical waters: ubiquitous occurrence of veterinary antibiotics in the Mekong delta. Environ Sci Technol 41:8004–8010. doi:10.1021/es0709021
Margesin R, Schinner F (1997) Bioremediation of diesel-oil-contaminated alpine soils at low temperatures. Appl Microbiol and Biot 47:462–468. doi:10.1007/s002530050957
Margesin R, Zimmerbauer A, Schinner F (2000) Monitoring of bioremediation by soil biological activities. Chemosphere 40:339–346. doi:10.1016/S0045-6535(99)00218-0
Matamoros V, Bayona JM (2006) Elimination of pharmaceuticals and personal care products in subsurface flow constructed wetlands. Environ Sci Technol 40(18):5811–5816. doi:10.1021/es0607741
Matamoros V, García J, Bayona JM (2008) Organic micropollutant removal in a full-scale surface flow constructed wetland fed with secondary effluent. Water Res 42(3):653–660. doi:10.1016/j.watres.2007.08.016
Matamoros V, Nguyen LX, Arias CA, Salvadó V, Brix H (2012) Evaluation of aquatic plants for removing polar microcontaminants: a microcosm experiment. Chemosphere 88:1257–1264. doi:10.1016/j.chemosphere.2012.04.004
Mei X, Yang Y, Tam NF, Li L, Wang YW (2014) Roles of root porosity, radial oxygen loss, Fe plaque formation on nutrient removal and tolerance of wetland plants to domestic wastewater. Water Res 50:147–159. doi:10.1016/j.watres.2013.12.004
Miao XS, Bishay F, Chen M, Metcalfe CD (2004) Occurrence of antimicrobials in the final effluents of wastewater treatment plants in Canada. Environ Sci Technol 38(13):3533–3541. doi:10.1021/es030653q
Nielsen JL, Nielsen PH (2002) Enumeration of acetate-consuming bacteria by microautoradiography under oxygen and nitrate respiring conditions in activated sludge. Water Res 36:421–428. doi:10.1016/S0167-5648(02)80027-2
Pi N, Tam N, Wong MH (2011) Formation of iron plaque on mangrove roots receiving wastewater and its role in immobilization of wastewater-borne pollutants [J]. Marine Pollut Bull 63(5):402–411. doi:10.1016/j.jhazmat.2012.02.056
Reichel R, Rosendahl I, Peeters E, Focks A, Groeneweg J, Bierl R, Schlichting A, Amelung W, Thiele-Bruhn S (2013) Effects of slurry from sulfadiazine- (SDZ) and difloxacin- (DIF) medicated pigs on the structural diversity of microorganisms in bulk and rhizosphere soil. Soil Biol Biochem 62:82–91. doi:10.1016/j.soilbio.2013.03.007
Reichel R, Radl V, Rosendahl I, Albert A, Amelung W, Schloter M, Thiele-Bruhn S (2014) Soil microbial community responses to antibiotic-contaminated manure under different soil moisture regimes. Appl Microbiol Biotechnol 98:6487–6495. doi:10.1007/s00253-014-5717-4
Reichel R, Michelini L, Ghisi R, Thiele-Bruhn S (2015) Soil bacterial community response to sulfadiazine in the soil–root zone. J Plant Nutr Soil Sci 178:499–506. doi:10.1002/jpln.201400352
Reinhold D, Vishwanathan S, Park JJ, Oh D, Michael SF (2010) Assessment of plant-driven removal of emerging organic pollutants by duckweed. Chemosphere 80:687–692. doi:10.1016/j.chemosphere.2010.05.045
Seeger EM, Reiche N, Kuschk P, Borsdorf H, Kaestner M (2011) Performance evaluation using a three compartment mass balance for the removal of volatile organic compounds in pilot scale constructed wetlands. Environ Sci Technol 45(19):8467–8474. doi:10.1021/es201536j
Shao B, Chen D, Zhang J, Wu YN, Sun CJ (2009) Determination of 76 pharmaceutical drugs by liquid chromatography-tandem mass spectrometry in slaughterhouse wastewater. J Chromatogr A 1216(47):8312–8318. doi:10.1016/j.chroma.2009.08.038
Silva-Costa C, Friães A, Ramirez M, Melo-Cristino J (2012) Differences between macrolide-resistant and -susceptible streptococcus pyogenes: importance of clonal properties in addition to antibiotic consumption. Antimicrob Agents Ch 56(11):5661–5666. doi:10.1128/AAC.01133-12
Su HC, Ying GG, Tao R, Zhang RQ, Zhao JL, Liu YS (2012) Class 1 and 2 integrons, sul resistance genes and antibiotic resistance in Escherichia coliisolated from Dongjiang River, South China. Environ Pollut 169:42–49. doi:10.1016/j.envpol.2012.05.007
Tang X, Wang S, Yang Y, Tao R, Dai Y, A D (2015) Removal of six phthalic acid esters (PAEs) from domestic sewage by constructed wetlands. Chem Eng J 275, 198–205. doi:10.1016/j.cej.2015.04.029
Tao R, Ying GG, Su HC, Zhou HW, Sidhu JPS (2010) Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the pearl rivers in South China. Environ Pollut 158:2101–2109. doi:10.1016/j.envpol.2010.03.004
Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70(8):1254–1257
Taylor G, Crowder A, Rodden R (1984) Formation and morphology of an iron plaque on the roots of Typha Latifolia L. grown in solution culture. Am J Bot 71:666–675. doi:10.2307/2443363
Tront JM, Saunders FM (2006) Role of plant activity and contaminant speciation in aquatic plant assimilation of 2, 4, 5-trichlorophenol. Chemosphere 64:400–407. doi:10.1016/j.chemosphere.2005.12.025
Vasiliadou I, Molina R, Martínez F, Melero J (2013) Biological removal of pharmaceutical and personal care products by a mixed microbial culture: sorption, desorption and biodegradation. Biochem Eng J 81:108–119. doi:10.1016/j.bej.2013.10.010
Weber K, Mitzel M, Slawson R (2011) Effect of ciprofloxacin on microbiological development in wetland mesocosms. Water Res 45(10):3185–3196. doi:10.1016/j.watres.2011.03.042
Weng SS, Ku KL, Lai HT (2012) The implication of mediators for enhancement of laccase oxidation of sulfonamide antibiotics. Bioresour Technol 113:259–264. doi:10.1016/j.biortech.2011.12.111
Wu H, Wang X, He X, Zhang S, Liang R, Shen J (2017) Effects of root exudates on denitrifier gene abundance, community structure and activity in a micro-polluted constructed wetland. Sci Total Environ 598:697–703. doi:10.1016/j.scitotenv.2017.04.150
Xu W, Zhang G, Li X et al (2007) Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD), South China. Water Res 41(19):4526–4534. doi:10.1016/j.watres.2007.06.023
Yang JF, Ying GG, Zhao JL, Tao R, Su HC, Liu YS (2011) Spatial and seasonal distribution of selected antibiotics in surface waters of the pearl rivers. China J Environ Sci Health B 46(3):272–280. doi:10.1080/03601234.2011.540540
Yang J, Tam NFY, Ye Z (2014) Root porosity, radial oxygen loss and iron plaque on roots of wetland plants in relation to zinc tolerance and accumulation. Plant Soil 374:815–828. doi:10.1007/s11104-013-1922-7
Ye Z, Weinberg H, Meyer M (2007) Trace analysis of trimethoprim and sulfonamide, macrolide, quinolone and tetracycline antibiotics in chlorinated drinking water using liquid chromatography electrospray tandem mass spectrometry. Analyt Chem 79:1135–1144. doi:10.1021/ac060972a
Zhang DQ, Hua T, Gersberg RM, Zhu J, Ng W, Tan SK (2013) Fate of caffeine in mesocosms wetland planted with Scirpus Validus. Chemosphere 90:1568. doi:10.1016/j.chemosphere.2012.09.059
Zhao C, Xie H, Xu J, Xu X, Zhang J, Hu Z, Liu C, Liang S, Wang Q (2015) Bacterial community variation and microbial mechanism of triclosan (TCS) removal by constructed wetlands with different types of plants. Sci Total Environ 505:633–639. doi:10.1016/j.scitotenv.2014.10.053
Zhou Q, Wu Z, Cheng S, He F, Fu G (2005) Enzymatic activities in constructed wetlands and di-n-phthalate (DBP) biodegradation. Soil Biol Biochem 37:1454–1459. doi:10.1016/j.soilbio.2005.01.003
Zurita F, De Anda J, Belmont MA (2009) Treatment of domestic wastewater and production of commercial flowers in vertical and horizontal subsurface-flow constructed wetlands. Ecol Eng 35:861–869. doi:10.1016/j.ecoleng.2008.12.026
Acknowledgments
We are also grateful to the National Natural Science Foundation of China (51509106, 51579115), the National Science Foundation for Post-doctoral Scientists of China (2015 M572410), the Natural Science Foundation of Guangdong Province (2016A030310097), and Pearl River S&T Nova Program of Guangzhou (201710010052), China for financial support.
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Tai, Y., Tam, N.FY., Dai, Y. et al. Assessment of rhizosphere processes for removing water-borne macrolide antibiotics in constructed wetlands. Plant Soil 419, 489–502 (2017). https://doi.org/10.1007/s11104-017-3359-x
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DOI: https://doi.org/10.1007/s11104-017-3359-x