Abstract
Purpose
To evaluate atrazine behavior in an agricultural soil (adsorption–desorption, leaching) and the effects of bioaugmentation with the Arthrobacter sp. strain AAC22, as a soil remediating strategy.
Material and methods
An agricultural soil with a history of atrazine application was used. Equilibrium batch experiments allowed the investigation of the adsorption–desorption of atrazine at different soil depths, while the atrazine leaching potential was assessed using disturbed soil columns. Arthrobacter sp. strain AAC22 was selected for bioaugmentation, to remove atrazine in soil microcosms. Removal efficiency was determined by a bioassay with oat seeds.
Results and discussion
Adsorption and desorption isotherms of atrazine at different soil depths were well described by the Freundlich equation (R2 > 0.99 and R2 > 0.98, respectively). The Freundlich constant (Kf) and desorption coefficient (Kfd1–3) decreased and increased, respectively, as soil depth increased. The Kf and Kfd1–3 values were correlated positively to organic carbon (r = 0.97) and negatively to pH (r = − 0.93). In this soil, 70.2% of atrazine applied (2.5 kg ha−1) was recovered in the leachate and 7.6% remained in the soil column. The higher atrazine concentration leached can be explained by the negative hysteresis of adsorption–desorption in this soil. Bioaugmentation with AAC22 enhanced atrazine removal being nearly 70% after 2 days of treatment, and it was almost complete (> 99%) after 8 days. A bioassay demonstrated that bioaugmentation was successful and toxic by-products were not detected.
Conclusion
The adsorption–desorption and leaching experiments demonstrated the high mobility of the atrazine in the study soil. The bioaugmentation using the AAC22 strain is an effective strategy for atrazine removal in polluted soils.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Albarrán A, Celis R, Hermosín MC, López-Piñeiro A, Ortega-Calvo JJ, Cornejo J (2003) Effects of solid olive-mill waste addition to soil on sorption, degradation and leaching of the herbicide simazine. Soil Use Manag 19:150–156. https://doi.org/10.1079/sum2002185
Alonso LL, Demetrio PM, Etchegoyen AM, Marino DJ (2018) Glyphosate and atrazine in rainfall and soils in agroproductive areas of the pampas region in Argentina. Sci Total Environ 645:89–96. https://doi.org/10.1016/j.scitotenv.2018.07.134
Alvarenga P, Palma P, Gonçalves AP, Fernandes RM, Cunha-Queda AC, Duarte E, Vallini G (2007) Evaluation of chemical and ecotoxicological characteristics of biodegradable organic residues for application to agricultural land. Environ Int 33(4):505–513. https://doi.org/10.1016/j.envint.2006.11.006
Amadori MF, Cordeiro GA, Rebouças CC, Peralta-Zamora PG, Grassi MT, Abate G (2013) Extraction method for the determination of atrazine, deethylatrazine, and deisopropylatrazine in agricultural soil using factorial design. J Braz Chem Soc 24(3):483–491. https://doi.org/10.5935/0103-5053.20130058
Aparicio JD, Saez JM, Raimondo EE, Benimeli CS, Polti MA (2018) Comparative study of single and mixed cultures of actinobacteria for the bioremediation of co-contaminated matrices. J Environ Chem Eng 6(2):2310–2318. https://doi.org/10.1016/j.jece.2018.03.030
Bachetti RA, Urseler N, Morgante V, Damilano G, Porporatto C, Agostini E, Morgante C (2021) Monitoring of atrazine pollution and its spatial-seasonal variation on surface water sources of an agricultural river basin. Bull Environ Contam Toxicol 106:929–935. https://doi.org/10.1007/s00128-021-03264-x
Barchanska H, Sajdak M, Szczypka K, Swientek A, Tworek M, Kurek M (2017) Atrazine, triketone herbicides, and their degradation products in sediment, soil and surface water samples in Poland. Environ Sci Pollut Res 24(1):644–658. https://doi.org/10.1007/s11356-016-7798-3
Barriuso E, Laird DA, Koskinen WC, Dowdy RH (1994) Atrazine desorption from smectites. Soil Sci Soc Am J 58:1632. https://doi.org/10.2136/sssaj1994.03615995005800060008x
Bedmar F, Costa JL, Suero E, Gimenez D (2004) Transport of atrazine and metribuzin in three soils of the humid pampas of Argentina. Weed Technol 18(1):1–8. https://doi.org/10.1614/WT-02-056
Bonfleur EJ, Tornisielo VL, Regitano JB, Lavorenti A (2015) The effects of glyphosate and atrazine mixture on soil microbial population and subsequent impacts on their fate in a tropical soil. Water Air Soil Pollut 226(2):1–10. https://doi.org/10.1007/s11270-014-2190-8
Chelinho S, Moreira-Santos M, Lima D, Silva C, Viana P, André S, Lopes I, Ribeiro R, Fialho AM, Viegas CA, Sousa JP (2010) Cleanup of atrazine-contaminated soils: ecotoxicological study on the efficacy of a bioremediation tool with Pseudomonas sp. ADP J Soils Sediments 10:568–578. https://doi.org/10.1007/s11368-009-0145-2
Daniel PE, Bedmar F, Costa JL, Aparicio VC (2002) Atrazine and metribuzin sorption in soils of the Argentinean humid pampas. Environ Toxicol Chem 21:2567–2572. https://doi.org/10.1002/etc.5620211207
De Gerónimo E, Aparicio VC, Bárbaro S, Portocarrero R, Jaime S, Costa JL (2014) Presence of pesticides in surface water from four sub-basins in Argentina. Chemosphere 107:423–431. https://doi.org/10.1016/j.chemosphere.2014.01.039
Delle SA (2001) Factors affecting sorption of organic compounds in natural sorbent/water systems and sorption coefficients for selected pollutants. A review. J Phys Chem Ref Data 30(1):187–439. https://doi.org/10.1063/1.1347984
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez LA, Tablada ME, Robledo CW (2019) InfoStat v. 2019. Cent. Transf. InfoStat, FCA, Univ. Nac. Córdoba, Argentina
Dinamarca MA, Cereceda-Balic F, Fadic X, Seeger M (2007) Analysis of s-triazine-degrading microbial communities in soils using most-probable-number enumeration and tetrazolium-salt detection. Int Microbiol 10:209–215. https://doi.org/10.2436/20.1501.01.29
EC (1998) European Commission Council Directive 98/83/EC. Off J Eur Comm 330:32–54
Epa US (2007) Atrazine - Chemical Summary. Publicacions Matem. https://doi.org/10.5565/PUBLMAT_Introduction
Fernandes AFT, Wang P, Staley C, Moretto JAS, Altarugio LM, Campanharo SC, Stehling EG, Sadowsky MJ (2020) Impact of atrazine exposure on the microbial community structure in a Brazilian tropical Latosol soil. Microbes Environ 35:1–7. https://doi.org/10.1264/jsme2.ME19143
Fernandez M, Paisio CE, Perotti R, Pereira PP, Agostini E, González PS (2019) Laboratory and field microcosms as useful experimental systems to study the bioaugmentation treatment of tannery effluents. J Environ Manage 234:503–511. https://doi.org/10.1016/j.jenvman.2019.01.019
Gee GW, Bauder JW (1979) Particle size analysis by hydrometer: a simplified method for routine textural analysis and a sensitivity test of measurement parameters. Soil Sci Soc Am J 43(5):1004–1007. https://doi.org/10.2136/sssaj1979.03615995004300050038x
Giles CH, MacEwan TH, Nakhwa SN, Smith D (1960) A system of classification of solution adsorption isotherms, and its use in diagnosis of adsorption mechanisms and in measurement of specific surface areas of solids. J Chem Soc 111:3973–3993. https://doi.org/10.1039/jr9600003973
Hang S, Nassetta M (2003) Evolución de la degradación de atrazina en dos perfiles de suelo de la provincia de Córdoba. Rev Investig Agropecu 32:57–69
Hang S, Sereno R (2002) Adsorción de atrazina y su relación con las caraterísticas sedimentológicas y el desarrollo del perfil de dos suelos de la provincia de Córdoba. Rev Investig Agropecu 31:73–87
Hansen AM, Treviño-Quintanilla LG, Márquez-Pacheco H, Villada-Canela M, Gonzalez-Marquez CL, Guillen-Garces AR, Hernandez-Antonio A (2013) Atrazine: a controversial herbicide. Rev Int Contam Ambient 29:65–84
Huang Y, Liu Z, He Y, Zeng F, Wang R (2013) Quantifying effects of primary parameters on adsorption-desorption of atrazine in soils. J Soils Sediments 13:82–93. https://doi.org/10.1007/s11368-012-0572-3
Huang Y, Liu Z, He Y, Li Y (2015) Impact of soil primary size fractions on sorption and desorption of atrazine on organo-mineral fractions. Environ Sci Pollut Res 22:4396–4405. https://doi.org/10.1007/s11356-014-3684-z
Inoue M, Oliveira R, Regitano J, Tormena CA, Constantin J, Tornisielo VL (2006) Sorption-desorption of atrazine and diuron in soils from southern Brazil. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes 41:605–621. https://doi.org/10.1080/03601230600701767
Jablonowski ND, Köppchen S, Hofmann D, Schäffer A, Burauel P (2009) Persistence of 14C-labeled atrazine and its residues in a field lysimeter soil after 22 years. Environ Pollut 157:2126–2131. https://doi.org/10.1016/j.envpol.2009.02.004
Kanissery R, Gairhe B, McAvoy C, Sims G (2019) Herbicide bioavailability determinant processes in the soil. J Bioremediation Biodegrad 10(458):2. https://doi.org/10.4172/2155-6199.1000458
Khan MA, Liang T (1989) Mapping pesticide contamination potential. Environ Manage 13:233–242. https://doi.org/10.1007/BF01868370
Komarova NV, Kartsova LA (2003) Determination of s-triazine herbicides by micellar electrokinetic chromatography using sodium dodecyl sulfate. J Anal Chem 58:785–789. https://doi.org/10.1023/A:1025099930530
Koskinen WC, Clay SA (1997) Factors affecting atrazine fate in north central U.S. soils. Rev Environ Contam Toxicol 117–165. https://doi.org/10.1007/978-1-4612-1958-3_4
Lima DLD, Schneider RJ, Scherer HW, Duarte AC, Santos EB, Esteves VI (2010) Sorption desorption behavior of atrazine on soils subjected to different organic long-term amendments. J Agric Food Chem 58:3101–3106. https://doi.org/10.1021/jf903937d
Mahía J, González-Prieto SJ, Martín A, Bååth E, Díaz-Raviña M (2011) Biochemical properties and microbial community structure of five different soils after atrazine addition. Biol Fertil Soils 47:577–589. https://doi.org/10.1007/s00374-011-0569-x
Martin-Neto L, Vieira EM, Sposito G (1994) Mechanism of atrazine sorption by humic acid: a spectroscopic study. Environ Sci Technol 28(11):1867–1873. https://doi.org/10.1021/es00060a017
Mendes KF, Shiroma AT, Pimpinato RF, Reis MR, Tornisielo VL (2019) Transport of atrazine via leaching in agricultural soil with mineral oil addition. Planta Daninha 37:1–7. https://doi.org/10.1590/S0100-83582019370100
Montoya JC, Costa JL, Liedl R, Bedmar F, Daniel P (2006) Effects of soil type and tillage practice on atrazine transport through intact soil cores. Geoderma 137:161–173. https://doi.org/10.1016/j.geoderma.2006.08.007
Morgante V, Flores C, Fadic X, González M, Hernández M, Cereceda-Balic F, Seeger M (2012) Influence of microorganisms and leaching on simazine attenuation in an agricultural soil. J Environ Manage 95:S300–S305. https://doi.org/10.1016/j.jenvman.2011.06.045
Morgante V, López-López A, Flores C, González M, González B, Vásquez M, Rosselló-Mora R, Seeger M (2010) Bioaugmentation with Pseudomonas sp. strain MHP41 promotes simazine attenuation and bacterial community changes in agricultural soils. FEMS Microbiol Ecol 71:114–126. https://doi.org/10.1111/j.1574-6941.2009.00790.x
Müller K, Duwig C, Prado B, Siebe C, Hidalgo C, Etchevers J (2012) Impact of long-term wastewater irrigation on sorption and transport of atrazine in Mexican agricultural soils. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes 47:30–41. https://doi.org/10.1080/03601234.2012.606416
OECD (2000) OECD Test Guideline 106: adsorption - desorption using a batch equilibrium method OECD Guidel Test Chem 1–44. https://doi.org/10.1787/9789264069602-en
OECD (2004) OECD Test Guideline 312: leaching in soil columns, OECD Guidelines for the Testing of Chemicals, Section 3. OECD Publishing, Paris. https://doi.org/10.1787/9789264070561-en
OECD (2006) OECD Test Guideline 208: terrestrial plant test - seedling emergence and seedling growth test. Guidel Test Chem Terr Plant Test Seedl. Emerg Seedl Growth Test. https://doi.org/10.1787/9789264070066-en
Paszko T, Muszyński P (2017) Degradation rates of alachlor, atrazine and bentazone in the profiles of Polish Luvisols. Int Agrophysics 31(3):401. https://doi.org/10.1515/intag-2016-0053
Ralebitso T, Senior E, Van Verseveld HW (2002) Microbial aspects of atrazine degradation in natural environments. Biodegradation V13:11–19. https://doi.org/10.1023/A:1016329628618
Rousseaux S, Hartmann A, Lagacherie B, Piutti S, Andreux F, Soulas G (2003) Inoculation of an atrazine-degrading strain, Chelatobacter heintzii Cit1, in four different soils: effects of different inoculum densities. Chemosphere 51(7):569–576. https://doi.org/10.1016/S0045-6535(02)00810-X
Rousseaux S, Hartmann A, Soulas G (2001) Isolation and characterisation of new Gram-negative and Gram-positive atrazine degrading bacteria from different French soils. FEMS Microbiol Ecol 36:211–222. https://doi.org/10.1016/S0168-6496(01)00135-0
Ruberto L, Mac Cormack W, Giulietti A, Merini L (2013) Microcosms: a key tool for the scaling up of soil bio/phytoremediation processes. In: Daniels J (ed) Advances in environmental research. Nova Publishers, New York, pp 201–228
Salazar-Ledesma M, Prado B, Zamora O, Siebe C (2018) Mobility of atrazine in soils of a wastewater irrigated maize field. Agric Ecosyst Environ 255:73–83. https://doi.org/10.1016/j.agee.2017.12.018
Silveira GL, Lima MGF, dos Reis GB, Palmieri MJ, Andrade-Vieria LF (2017) Toxic effects of environmental pollutants: comparative investigation using Allium cepa L. and Lactuca sativa L. Chemosphere 178:359–367. https://doi.org/10.1016/j.chemosphere.2017.03.048
Singh AK, Cameotra SS (2013) Adsorption and desorption behavior of chlorotriazine herbicides in the agricultural soils. J Pet Environ Biotechnol 4:5. https://doi.org/10.4172/2157-7463.1000154
Singh S, Kumar V, Chauhan A, Datta S, Wani AB, Singh N, Singh J (2018) Toxicity, degradation and analysis of the herbicide atrazine. Environ Chem Lett 16:211–237. https://doi.org/10.1007/s10311-017-0665-8
Sokolowski AC, Prack McCormick B, De Grazia J, Wolski JE, Rodríguez HA, Rodríguez-Frers EP, Gagey MC, Debelis SP, Paladino IR, Barrios MB (2020) Tillage and no-tillage effects on physical and chemical properties of an Argiaquoll soil under long-term crop rotation in Buenos Aires, Argentina. Int Soil Water Conserv Res 8:185–194. https://doi.org/10.1016/j.iswcr.2020.02.002
Stipičević S, Galzina N, Udiković-Kolić N, Jurina T, Mendaš G, Dvoršćak M, Petrić I, Barić K, Drevenkar V (2015) Distribution of terbuthylazine and atrazine residues in crop-cultivated soil: the effect of herbicide application rate on herbicide persistence. Geoderma 259:300–309. https://doi.org/10.1016/j.geoderma.2015.06.018
Struthers JK, Jayachandran K, Moorman TB (1998) Biodegradation of atrazine by Agrobacterium radiobacter J14a and use of this strain in bioremediation of contaminated soil. Appl Environ Microbiol 64:3368–3375. https://doi.org/10.1128/aem.64.9.3368-3375.1998
Sun J, Ma X, Wang W, Zhang J, Zhang H, Wang YJ, Feng J (2019) The adsorption behavior of atrazine in common soils in Northeast China. Bull Environ Contam Toxicol 103:316–322. https://doi.org/10.1007/s00128-019-02671-5
Süsse H, Müller H (1996) Pesticide analysis by micellar electrokinetic capillary chromatography. J Chromatogr A 730(1–2):337–343. https://doi.org/10.1016/0021-9673(95)01038-6
USDA (2014) Keys to soil taxonomy. Soil Conserv Serv. https://doi.org/10.1109/TIP.2005.854494
USDA NRCS (1999) United States Department of Agriculture Natural Resources Conservation Service. Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. USDA Nat Resour Conserv Serv
Vega RC, Camacho AGR, Sampieri A, Flores VT, Moreno RDP, Gómez SES (2021) Movilidad de atrazina en dos tipos de suelo en el estado de Puebla. Rev Mex Ciencias Agrícolas 12:291–304. https://doi.org/10.29312/remexca.v12i2.2425
Vryzas Z, Papadakis EN, Vassiliou G, Papadopoulou-Mourkidou E (2012) Occurrence of pesticides in transboundary aquifers of North-eastern Greece. Sci Total Environ 441:41–48. https://doi.org/10.1016/j.scitotenv.2012.09.074
Vryzas Z, Papadopoulou-Mourkidou E, Soulios G, Prodromou K (2007) Kinetics and adsorption of metolachlor and atrazine and the conversion products (deethylatrazine, deisopropylatrazine, hydroxyatrazine) in the soil profile of a river basin. Eur J Soil Sci 58:1186–1199. https://doi.org/10.1111/j.1365-2389.2007.00913.x
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38. https://doi.org/10.1097/00010694-193401000-00003
Wang Q, Xie S, Hu R (2013) Bioaugmentation with Arthrobacter sp. strain DAT1 for remediation of heavily atrazine-contaminated soil. Int Biodeterior Biodegrad 77:63–67. https://doi.org/10.1016/j.ibiod.2012.11.003
Yang Y, Cao H, Peng P, Bo H (2014) Degradation and transformation of atrazine under catalyzed ozonation process with TiO2 as catalyst. J Hazard Mater 279:444–451. https://doi.org/10.1016/j.jhazmat.2014.07.035
Yue L, Ge CJ, Feng D, Yu H, Deng H, Fu B (2017) Adsorption–desorption behavior of atrazine on agricultural soils in China. J Environ Sci (china) 57:180–189. https://doi.org/10.1016/j.jes.2016.11.002
Zhang Y, Ge S, Jiang M, Jiang Z, Wang Z, Ma B (2014) Combined bioremediation of atrazine-contaminated soil by Pennisetum and Arthrobacter sp. strain DNS10. Environ Sci Pollut Res 21:6234–6238. https://doi.org/10.1007/s11356-013-2410-6
Zhou X, Wang Q, Wang Z, Xie S (2013) Nitrogen impacts on atrazine-degrading Arthrobacter strain and bacterial community structure in soil microcosms. Environ Sci Pollut Res 20:2484–2491. https://doi.org/10.1007/s11356-012-1168-6
Zhu J, Zhao Y, Fu L, Liu Z, Li X, Meng Z (2020) Application of a simazine degrading bacterium, Arthrobacter ureafaciens XMJZ01 for bioremediation of simazine pollution. Water Environ J 0:1-12. https://doi.org/10.1111/wej.12560
Zucconi F, Monaco A, Forte M (1984) Phytotoxins during the stabilization of organic matter. Composting of agricultural and other wastes. Elsevier, London, pp 73–86
Zucconi F, Pera A, Forte M, De Bertoldi M (1981) Evaluating toxicity of immature compost. Biocycle 22:54–57
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NU holds a doctoral grant from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). This work was carried out with financial support from FONCyT (grant PICT Start up 0018/2016) and Instituto de Investigación, Universidad Nacional de Villa María. EA is a member of CONICET.
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This research was financed by FONCyT (grant PICT Start up 0018/2016) and by the Instituto de Investigación, Universidad Nacional de Villa María (grant UNVM resolution N° 614/2018).
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NU, RB, VM, EA, and CM conceived and designed the research. NU, RB, and VM contributed with material preparation, data collection, and analysis. NU and EA wrote the draft manuscript. All the authors read and approved the final manuscript.
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Urseler, N., Bachetti, R., Morgante, V. et al. Atrazine behavior in an agricultural soil: adsorption–desorption, leaching, and bioaugmentation with Arthrobacter sp. strain AAC22. J Soils Sediments 22, 93–108 (2022). https://doi.org/10.1007/s11368-021-03045-3
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DOI: https://doi.org/10.1007/s11368-021-03045-3