Abstract
An experimental study evaluating the effect of bioaugmentation and antibiotic (oxytetracycline) application on pesticide degradation and microbial community structure of a biomixture used in a biopurification system (BPR) was conducted. The bioaugmentation employed a carbofuran-degrading bacterial consortium. The non-bioaugmented biomixture showed excellent performance for removal of atrazine (t1/2: 9.9 days), carbendazim (t1/2: 3.0 days), carbofuran (t1/2: 2.8 days), and metalaxyl (t1/2: 2.7 days). Neither the addition of oxytetracycline nor bioaugmentation affected the efficiency of pesticide removal or microbial community (bacterial and fungal) structure, as determined by DGGE analysis. Instead, biomixture aging was mainly responsible for microbial population shifts. Even though the bioaugmentation did not enhance the biomixtures′ performance, this matrix showed a high capability to sustain initial stresses related to antibiotic addition; therefore, simultaneous elimination of this particular mixture of pesticides together with oxytetracycline residues is not discouraged.
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References
Arbeli Z, Fuentes CL (2007) Accelerated biodegradation of pesticides: an overview of the phenomenon, its basis and possible solutions; and a discussion on the tropical dimension. Crop Prot 26(12):1733–1746. https://doi.org/10.1016/j.cropro.2007.03.009
Boleas S, Alonso C, Pro J, Fernández C, Carbonell G, Tarazona JV (2005) Toxicity of the antimicrobial oxytetracycline to soil organisms in a multi-species-soil system (MS· 3) and influence of manure co-addition. J Hazard Mater 122(3):233–241. https://doi.org/10.1016/j.jhazmat.2005.03.003
Bouchez T, Patureau D, Dabert P, Juretschko S, Dore J, Delgenes P, Moletta R, Wagner M (2000) Ecological study of a bioaugmentation failure. Environ Microbiol 2(2):179–190. https://doi.org/10.1046/j.1462-2920.2000.00091.x
Briceño G, Rubilar O, Tortella G (2013) Bioaumentación de una biomezcla con actinobacterias degradadoras de residuos de plaguicidas organofosforados. In Workshop Internacional y Taller Nacional Valorización. Pucón, Chile
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267. https://doi.org/10.1093/bioinformatics/btp636
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez-Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh P.J, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5): 335–336. https://doi.org/10.1038/nmeth.f.303
Castillo MDP, Torstensson L, Stenström J (2008) Biobeds for environmental protection from pesticide use. A review. J Agric Food Chem 56(15):6206–6219. https://doi.org/10.1021/jf800844x
Castillo-Díaz JMC, Delgado-Moreno L, Núñez R, Nogales R, Romero E (2016) Enhancing pesticide degradation using indigenous microorganisms isolated under high pesticide load in bioremediation systems with vermicomposts. Bioresour Technol 214:234–241. https://doi.org/10.1016/j.biortech.2016.04.105
Castro-Gutiérrez V, Masís-Mora M, Caminal G, Vicent T, Carazo-Rojas E, Mora-López M, Rodríguez-Rodríguez CE (2016) A microbial consortium from a biomixture swiftly degrades high concentrations of carbofuran in fluidized-bed reactors. Process Biochem 51(10):1585–1593. https://doi.org/10.1016/j.procbio.2016.07.003
Castro-Gutiérrez V, Masís-Mora M, Diez MC, Tortella GR, Rodríguez-Rodríguez CE (2017) Aging of biomixtures: effects on carbofuran removal and microbial community structure. Chemosphere 168:418–425. https://doi.org/10.1016/j.chemosphere.2016.10.065
Chin-Pampillo JS, Carazo-Rojas E, Pérez-Rojas G, Castro-Gutiérrez V, Rodríguez-Rodríguez CE (2015a) Accelerated biodegradation of selected nematicides in tropical crop soils from Costa Rica. Environ Sci Pollut Res 22(2):1240–1249. https://doi.org/10.1007/s11356-014-3414-6
Chin-Pampillo JS, Ruiz-Hidalgo K, Masís-Mora M, Carazo-Rojas E, Rodríguez-Rodríguez CE (2015b) Adaptation of biomixtures for carbofuran degradation in on-farm biopurification systems in tropical regions. Environ Sci Pollut Res 22(13):9839–9848. https://doi.org/10.1007/s11356-015-4130-6
Chin-Pampillo JS, Ruiz-Hidalgo K, Masís-Mora M, Carazo-Rojas E, Rodríguez-Rodríguez CE (2015c) Design of an optimized biomixture for the degradation of carbofuran based on pesticide removal and toxicity reduction of the matrix. Environ Sci Pollut Res 22(23):19184–19193. https://doi.org/10.1007/s11356-015-5093-3
Chu B, Eivazi F (2015) Enhancing biodegradation of herbicides using biobed systems. J Environ Indicators 9:32–33
Coppola L, Castillo P, Vischetti C (2011) Degradation of isoproturon and bentazone in peat- and compost-based biomixtures. Pest Manag Sci 67(1):107–113. https://doi.org/10.1002/ps.2040
Dai Y, Li N, Zhao Q, Xie S (2015) Bioremediation using Novosphingobium strain DY4 for 2, 4-dichlorophenoxyacetic acid-contaminated soil and impact on microbial community structure. Biodegradation 26(2):161–170. https://doi.org/10.1007/s10532-015-9724-7
Dejonghe W, Goris J, El Fantroussi S, Höfte M, De Vos P, Verstraete W, Top EM (2000) Effect of dissemination of 2, 4-dichlorophenoxyacetic acid (2, 4-D) degradation plasmids on 2, 4-D degradation and on bacterial community structure in two different soil horizons. Appl Environ Microbiol 66(8):3297–3304. https://doi.org/10.1128/AEM.66.8.3297-3304.2000
Desaint S, Hartmann A, Parekh NR, Fournier JC (2000) Genetic diversity of carbofuran-degrading soil bacteria. FEMS Microb Ecol 34(2):173–180. https://doi.org/10.1111/j.1574-6941.2000.tb00767.x
Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 87(3):925–941. https://doi.org/10.1007/s00253-010-2649-5
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Fogg P, Boxall AB, Walker A (2003) Degradation of pesticides in biobeds: the effect of concentration and pesticide mixtures. J Agric Food Chem 51(18):5344–5349. https://doi.org/10.1021/jf030060z
Goldstein RM, Mallory LM, Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Appl Environ Microbiol 50(4):977–983
Goux S, Shapir N, El Fantroussi S, Lelong S, Agathos SN, Pussemier L (2003) Long-term maintenance of rapid atrazine degradation in soils inoculated with atrazine degraders. Water Air Soil Pollut 3(3):131–142. https://doi.org/10.1023/A:1023998222016
Huete-Soto A, Castillo-González H, Masís-Mora M, Chin-Pampillo JS, Rodríguez-Rodríguez CE (2017a) Effects of oxytetracycline on the performance and activity of biomixtures: removal of herbicides and mineralization of chlorpyrifos. J Hazard Mater 321:1–8. https://doi.org/10.1016/j.jhazmat.2016.08.078
Huete-Soto A, Masís-Mora M, Lizano-Fallas V, Chin-Pampillo JS, Carazo-Rojas E, Rodríguez-Rodríguez CE (2017b) Simultaneous removal of structurally different pesticides in a biomixture: detoxification and effect of oxytetracycline. Chemosphere 169:558–567. https://doi.org/10.1016/j.chemosphere.2016.11.106
Hund-Rinke K, Simon M, Lukow T (2004) Effects of tetracycline on the soil microflora: function, diversity, resistance. J Soils Sediments 4(1):11–16. https://doi.org/10.1007/BF02990823
Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72(3):1719–1728. https://doi.org/10.1128/AEM.72.3.1719-1728.2006
Jiménez-Gamboa D, Castro-Gutiérrez V, Fernández-Fernández E, Briceño-Guevara S, Masís-Mora M, Chin-Pampillo J, Mora-López M, Carazo-Rojas E, Rodríguez-Rodríguez CE (2018) Expanding the application scope of on-farm biopurification systems: effect and removal of oxytetracycline in a biomixture. J Hazard Mater 342:553–560. https://doi.org/10.1016/j.jhazmat.2017.08.059
Karpouzas DG, Morgan JAW, Walker A (2000) Isolation and characterization of 23 carbofuran-degrading bacteria from soils from distant geographical areas. Lett Appl Microbiol 31(5):353–358. https://doi.org/10.1046/j.1472-765x.2000.00823.x
Karpouzas DG, Walker A, Drennan DSH, Froud-Williams RJ (2001) The effect of initial concentration of carbofuran on the development and stability of its enhanced biodegradation in top-soil and sub-soil. Pest Manag Sci 57(1):72–81. https://doi.org/10.1002/1526-4998(200101)57:1<72::AID-PS264>3.0.CO;2-1
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2012) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41(1):e1
Krutz LJ, Zablotowicz RM, Reddy KN, Koger Iii CH, Weaver MA (2007) Enhanced degradation of atrazine under field conditions correlates with a loss of weed control in the glasshouse. Pest Manag Sci 63(1):23–31. https://doi.org/10.1002/ps.1304
Kümmerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75(4):417–434. https://doi.org/10.1016/j.chemosphere.2008.11.086
Lewis KA, Tzilivakis J, Warner DJ, Green A (2016) An international database for pesticide risk assessments and management. Hum Ecol Risk Assess 22(4):1050–1064. https://doi.org/10.1080/10807039.2015.1133242
Marinozzi M, Coppola L, Monaci E, Karpouzas DG, Papadopoulou E, Menkissoglu-Spiroudi U, Vischetti C (2013) The dissipation of three fungicides in a biobed organic substrate and their impact on the structure and activity of the microbial community. Environ Sci Pollut Res 20(4):2546–2555. https://doi.org/10.1007/s11356-012-1165-9
Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73(1):127–141. https://doi.org/10.1023/A:1000669317571
Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic Press, San Diego
Robertson BK, Alexander M (1994) Growth-linked and cometabolic biodegradation: possible reason for occurrence or absence of accelerated pesticide biodegradation. Pestic Sci 41(4):311–318. https://doi.org/10.1002/ps.2780410405
Rodríguez-Rodríguez CE, Castro-Gutiérrez V, Chin-Pampillo JS, Ruiz-Hidalgo K (2013) On-farm biopurification systems: role of white rot fungi in depuration of pesticide-containing wastewaters. FEMS Microbiol Lett 345(1):1–12. https://doi.org/10.1111/1574-6968.12161
Ruiz-Hidalgo K, Chin-Pampillo JS, Masís-Mora M, Carazo E, Rodríguez-Rodríguez CE (2014) Degradation of carbofuran by Trametes versicolor in rice husk as a potential lignocellulosic substrate for biomixtures: from mineralization to toxicity reduction. Process Biochem 49(12):2266–2271. https://doi.org/10.1016/j.procbio.2014.10.006
Schmitt H, Haapakangas H, Van Beelen P (2005) Effects of antibiotics on soil microorganisms: time and nutrients influence pollution-induced community tolerance. Soil Biol Biochem 37(10):1882–1892. https://doi.org/10.1016/j.soilbio.2005.02.022
Shin DH, Kim DU, Seong CN, Song HG, Ka JO (2012) Genetic and phenotypic diversity of carbofuran-degrading bacteria isolated from agricultural soils. J Microbiol Biotechnol 22(4):448–456. https://doi.org/10.4014/jmb.1108.08087
Singh BK, Walker A, Wright DJ (2002) Degradation of chlorpyrifos, fenamiphos, and chlorothalonil alone and in combination and their effects on soil microbial activity. Environ Toxicol Chem 21(12):2600–2605. https://doi.org/10.1002/etc.5620211211
Sniegowski K, Bers K, Van Goetem K, Ryckeboer J, Jaeken P, Spanoghe P, Springael D (2011) Improvement of pesticide mineralization in on-farm biopurification systems by bioaugmentation with pesticide-primed soil. FEMS Microb Ecol 76(1):64–73. https://doi.org/10.1111/j.1574-6941.2010.01031.x
Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194(16):4151–4160. https://doi.org/10.1128/JB.00345-12
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(9):3368–3375
Tortella GR, Mella-Herrera RA, Sousa DZ, Rubilar O, Acuña JJ, Briceño G, Diez MC (2013a) Atrazine dissipation and its impact on the microbial communities and community level physiological profiles in a microcosm simulating the biomixture of on-farm biopurification system. J Hazard Mater 260:459–467. https://doi.org/10.1016/j.jhazmat.2013.05.059
Tortella GR, Mella-Herrera RA, Sousa DZ, Rubilar O, Briceño G, Parra L, Diez MC (2013b) Carbendazim dissipation in the biomixture of on-farm biopurification systems and its effect on microbial communities. Chemosphere 93(6):1084–1093. https://doi.org/10.1016/j.chemosphere.2013.05.084
Vandermaesen J, Horemans B, Bers K, Vandermeeren P, Herrmann S, Sekhar A, Seuntjens P, Springael D (2016) Application of biodegradation in mitigating and remediating pesticide contamination of freshwater resources: state of the art and challenges for optimization. Appl Microbiol Biotechnol 100(17):7361–7376. https://doi.org/10.1007/s00253-016-7709-z
Verhagen P, De Gelder L, Boon N (2013) Inoculation with a mixed degrading culture improves the pesticide removal of an on-farm biopurification system. Curr Microbiol 67(4):466–471. https://doi.org/10.1007/s00284-013-0389-3
Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73(7):1163–1172. https://doi.org/10.1351/pac200173071163
Vidaver AK (2002) Uses of antimicrobials in plant agriculture. Clin Infect Dis 34(Supplement 3):S107–S110. https://doi.org/10.1086/340247
Wan R, Yang Y, Sun W, Wang Z, Xie S (2014) Simazine biodegradation and community structures of ammonia-oxidizing microorganisms in bioaugmented soil: impact of ammonia and nitrate nitrogen sources. Environ Sci Pollut Res 21(4):3175–3181. https://doi.org/10.1007/s11356-013-2268-7
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
Youssef NH, Elshahed MS (2009) Diversity rankings among bacterial lineages in soil. ISME J 3(3):305–313. https://doi.org/10.1038/ismej.2008.106
Yu Y, Chu X, Pang G, Xiang Y, Fang H (2009) Effects of repeated applications of fungicide carbendazim on its persistence and microbial community in soil. J Environ Sci 21(2):179–185. https://doi.org/10.1016/S1001-0742(08)62248-2
Zablotowicz RM, Weaver MA, Locke MA (2006) Microbial adaptation for accelerated atrazine mineralization/degradation in Mississippi Delta soils. Weed Sci 54(3):538–547. https://doi.org/10.1614/WS-04-179R3.1
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This work was supported by Vicerrectoría de Investigación, Universidad de Costa Rica (project 802-B4-503), and the Costa Rican Ministry of Science, Technology and Telecommunications, MICITT (project FI-093-13).
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Castro-Gutiérrez, V., Masís-Mora, M., Carazo-Rojas, E. et al. Impact of oxytetracycline and bacterial bioaugmentation on the efficiency and microbial community structure of a pesticide-degrading biomixture. Environ Sci Pollut Res 25, 11787–11799 (2018). https://doi.org/10.1007/s11356-018-1436-1
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DOI: https://doi.org/10.1007/s11356-018-1436-1