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Microbial population shift caused by sulfamethoxazole in engineered-Soil Aquifer Treatment (e-SAT) system

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Abstract

The engineered-Soil Aquifer Treatment (e-SAT) system was exploited for the biological degradation of Sulfamethoxazole (SMX) which is known to bio-accumulate in the environment. The fate of SMX in soil column was studied through laboratory simulation for a period of 90 days. About 20 ppm SMX concentration could be removed in four consecutive cycles in e-SAT. To understand the microbial community change and biological degradation of SMX in e-SAT system, metagenomic analysis was performed for the soil samples before (A-EBD) and after SMX exposure (B-EBD) in the e-SAT. Four bacterial phyla were found to be present in both the samples, with sample B-EBD showing increased abundance for Actinobacteria, Bacteroidetes, Firmicutes and decreased Proteobacterial abundance compared to A-EBD. The unclassified bacteria were found to be abundant in B-EBD compared to A-EBD. At class level, classes such as Bacilli, Negativicutes, Deltaproteobacteria, and Bacteroidia emerged in sample B-EBD owing to SMX treatment, while Burkholderiales and Nitrosomonadales appeared to be dominant at order level after SMX treatment. Furthermore, in response to SMX treatment, the family Nitrosomonadaceae appeared to be dominant. Pseudomonas was the most dominating bacterial genus in A-EBD whereas Cupriavidus dominated in sample B-EBD. Additionally, the sulfur oxidizing bacteria were enriched in the B-EBD sample, signifying efficient electron transfer and hence organic molecule degradation in the e-SAT system. Results of this study offer new insights into understanding of microbial community shift during the biodegradation of SMX.

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References

  • Aga DS (2007) Fate of pharmaceuticals in the environment and in water treatment systems. CRC Press 86–87

  • Alidina M, Li D, Drewes JE (2014) Investigating the role for adaptation of the microbial community to transform trace organic chemicals during managed aquifer recharge. Water Res 56:172–180

    Article  CAS  Google Scholar 

  • Andreozzi R, Canterino M, Marotta R, Paxeus N (2005) Antibiotic removal from wastewaters: the ozonation of amoxicillin. J Hazard Mater 122:243–250

    Article  CAS  Google Scholar 

  • Avisar D, Lester Y, Mamane H (2010) pH induced polychromatic UV treatment for the removal of a mixture of SMX, OTC and CIP from water. J Hazard Mater 175:1068–1074

    Article  CAS  Google Scholar 

  • Batt AL, Kim S, Aga DS (2007) Comparison of the occurrence of antibiotics in four full-scale wastewater treatment plants with varying designs and operations. Chemosphere 68:428–435

    Article  CAS  Google Scholar 

  • Baumgarten B, Jahrig J, Reemtsma T, Jekel M (2011) Long term laboratory column experiments to simulate bank filtration: factors controlling removal of sulfamethoxazole. Water Res 45:211–220

    Article  CAS  Google Scholar 

  • Benotti MJ, Trenholm RA, Vanderford BJ, Holady JC, Stanford BD, Snyder SA (2008) Pharmaceuticals and endocrine disrupting compounds in US drinking water. Environ Sci Technol 43:597–603

    Article  Google Scholar 

  • Blake GR (1965) Bulk density. Methods Soil Anal 374–390

  • Bouju H, Ricken B, Beffa T, Corvini PFX, Kolvenbach BA (2012) Isolation of bacterial strains capable of sulfamethoxazole mineralization from an acclimated membrane bioreactor. Appl Environ Microb 78:277–279

    Article  CAS  Google Scholar 

  • Bruce GM, Pleus RC, Snyder SA (2010) Toxicological relevance of pharmaceuticals in drinking water. Environ Sci Technol 44:5619–5626

    Article  CAS  Google Scholar 

  • Collado N, Buttiglieri G, Marti E, Ferrando-Climent L, Rodriguez-Mozaz S, Barceló D, Rodriguez-Roda I (2013) Effects on activated sludge bacterial community exposed to sulfamethoxazole. Chemosphere 93:99–106

    Article  CAS  Google Scholar 

  • Deng Y, Mao Y, Li B, Yang C, Zhang T (2016) Aerobic degradation of sulfadiazine by Arthrobacter spp.: kinetics, pathways, and genomic characterization. Environ Sci Technol 50:9566–9575

    Article  CAS  Google Scholar 

  • Drillia P, Dokianakis SN, Fountoulakis MS, Kornaros M, Stamatelatou K, Lyberatos G (2005) On the occasional biodegradation of pharmaceuticals in the activated sludge process: the example of the antibiotic sulfamethoxazole. J Hazard Mater 122:259–265

    Article  CAS  Google Scholar 

  • Famiglietti JS, Rudnicki JW, Rodell M (1998) Variability in surface moisture content along a hillslope transect: Rattlesnake Hill, Texas. J Hydrol 210:259–281

    Article  Google Scholar 

  • Gao S, Zhao Z, Xu Y, Tian J, Qi H, Lin W, Cui F (2014) Oxidation of sulfamethoxazole (SMX) by chlorine, ozone and permanganate: a comparative study. J Hazard Mater 274:258–269

    Article  CAS  Google Scholar 

  • Gonzalez O, Esplugas M, Sans C, Esplugas S (2008) Biodegradation of photo-Fenton pre-treated solutions of Sulfamethoxazole by aerobic communities. Molecular biology techniques applied to the determination of existing strains. J Adv Oxid Technol 11:238–245

    CAS  Google Scholar 

  • Guizani M, Kato H, Funamizu N (2011) Assessing the removal potential of soil-aquifer treatment system (soil column) for endotoxin. J Environ Monitor 13:1716–1722

    Article  CAS  Google Scholar 

  • He K, Echigo S, Itoh S (2016) Effect of operating conditions in soil aquifer treatment on the removals of pharmaceuticals and personal care products. Sci Total Environ 565:672–681

    Article  CAS  Google Scholar 

  • Herzog B, Lemmer H, Horn H, Müller E (2013) Characterization of pure cultures isolated from sulfamethoxazole-acclimated activated sludge with respect to taxonomic identification and sulfamethoxazole biodegradation potential. BMC Microbiol 13:1

    Article  Google Scholar 

  • Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice Hall of India Pvt. Ltd, New Delhi 41–234

    Google Scholar 

  • Jiang B, Cui D, Li A, Gai Z, Ma F, Yang J, Ren N (2012) Genome sequence of a cold-adaptable sulfamethoxazole-degrading bacterium, Pseudomonas psychrophila HA-4. J Bacteriol 194:5721–5721

    Article  CAS  Google Scholar 

  • Jiang B, Li A, Cui D, Cai R, Ma F, Wang Y (2014) Biodegradation and metabolic pathway of sulfamethoxazole by Pseudomonas psychrophila HA-4, a newly isolated cold-adapted sulfamethoxazole-degrading bacterium. Appl Microbiol Biot 98:4671–4681

    Article  CAS  Google Scholar 

  • Kummerer K, Henninger A (2003) Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin Microbiol Infect 9:1203–1214

    Article  CAS  Google Scholar 

  • Larcher S, Yargeau V (2011) Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biot 91:211–218

    Article  CAS  Google Scholar 

  • Lian J, Luo Z, Jin M (2013) Transport and fate of bacteria in SAT system recharged with recycling water. Int Biodeterior Biodegradation 76:98–101

    Article  CAS  Google Scholar 

  • Marshall KT, Morris RM (2013) Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic 96BD-19 clade. ISME J 7:452–455

    Article  CAS  Google Scholar 

  • Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J (2008) The metagenomics RAST server: a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386

    Article  CAS  Google Scholar 

  • More RP, Mitra S, Raju SC, Kapley A, Purohit HJ (2014) Mining and assessment of catabolic pathways in the metagenome of a common effluent treatment plant to induce the degradative capacity of biomass. Bioresour Technol 153:137–146

    Article  CAS  Google Scholar 

  • Muller H, Bosch J, Griebler C, Damgaard LR, Nielsen LP, Lueders T, Meckenstock RU (2016) Long-distance electron transfer by cable bacteria in aquifer sediments. ISME J 10:2010–2019

    Article  Google Scholar 

  • Nakada N, Yasojima M, Okayasu Y, Komori K, Suzuki Y (2010) Mass balance analysis of triclosan, diethyltoluamide, crotamiton and carbamazepine in sewage treatment plants. Water Sci Technol 61:1739–1747

    Article  CAS  Google Scholar 

  • Oliveros JC (2009) Venny. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html

  • Onesios KM, Bouwer EJ (2012) Biological removal of pharmaceuticals and personal care products during laboratory soil aquifer treatment simulation with different primary substrate concentrations. Water Res 46:2365–2375

    Article  CAS  Google Scholar 

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    Article  CAS  Google Scholar 

  • Peng X, Tan J, Tang C, Yu Y, Wang Z (2008) Multiresidue determination of fluoroquinolone, sulfonamide, trimethoprim, and chloramphenicol antibiotics in urban waters in China. Environ Toxicol Chem 27:73–79

    Article  CAS  Google Scholar 

  • Peng X, Zhang K, Tang C, Huang Q, Yu Y, Cui J (2011) Distribution pattern, behavior, and fate of antibacterials in urban aquatic environments in South China. J Environ Monitor 13:446–454

    Article  CAS  Google Scholar 

  • Reis PJ, Reis AC, Ricken B, Kolvenbach BA, Manaia CM, Corvini PF, Nunes OC (2014) Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1. J Hazard Mater 280:741–749

    Article  CAS  Google Scholar 

  • Rivas FJ, Beltrán FJ, Encinas A (2012) Removal of emergent contaminants: integration of ozone and photocatalysis. J Environ Manage 100:10–15

    Article  CAS  Google Scholar 

  • Rodayan A, Roy R, Yargeau V (2010) Oxidation products of sulfamethoxazole in ozonated secondary effluent. J Hazard Mater 177:237–243

    Article  CAS  Google Scholar 

  • Rodriguez-Escales P, Sanchez-Vila X (2016) Fate of sulfamethoxazole in groundwater: conceptualizing and modeling metabolite formation under different redox conditions. Water Res 105:540–550

    Article  CAS  Google Scholar 

  • Schaffer M, Kroger KF, Nodler K, Ayora C, Carrera J, Hernandez M, Licha T (2015) Influence of a compost layer on the attenuation of 28 selected organic micropollutants under realistic soil aquifer treatment conditions: insights from a large scale column experiment. Water Res 74:110–121

    Article  CAS  Google Scholar 

  • Szczepanowski R, Linke B, Krahn I, Gartemann KH, Gutzkow T, Eichler W, Puhler A, Schluter A (2009) Detection of 140 clinically relevant antibiotic resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 155:2306–2319

    Article  CAS  Google Scholar 

  • Valhondo C, Carrera J, Ayora C, Tubau I, Martinez-Landa L, Nodler K, Licha T (2015) Characterizing redox conditions and monitoring attenuation of selected pharmaceuticals during artificial recharge through a reactive layer. Sci Tot Environ 512:240–250

    Article  Google Scholar 

  • Wang L, Liu Y, Ma J, Zhao F (2016) Rapid degradation of sulphamethoxazole and the further transformation of 3-amino-5-methylisoxazole in a microbial fuel cell. Water Res 88:322–328

    Article  CAS  Google Scholar 

  • Wei L, Li S, Noguera DR, Qin K, Jiang J, Zhao Q, Cui F (2015) Dissolved organic matter removal during coal slag additive soil aquifer treatment for secondary effluent recharging: contribution of aerobic biodegradation. J Environ Manage 156:158–166

    Article  CAS  Google Scholar 

  • Yadav TC, Pal RR, Shastri S, Jadeja NB, Kapley A (2015) Comparative metagenomics demonstrating different degradative capacity of activated biomass treating hydrocarbon contaminated wastewater. Bioresour Technol 188:24–32

    Article  CAS  Google Scholar 

  • Yafa C, Farmer JG (2006) A comparative study of acid-extractable and total digestion methods for the determination of inorganic elements in peat material by inductively coupled plasma-optical emission spectrometry. Anal Chim Acta 557:296–303

    Article  CAS  Google Scholar 

  • Yan C, Dinh QT, Chevreuil M, Garnier J, Roose-Amsaleg C, Labadie P, Laverman AM (2013) The effect of environmental and therapeutic concentrations of antibiotics on nitrate reduction rates in river sediment. Water Res 47:3654–3662

    Article  CAS  Google Scholar 

  • Yu K, Zhang T (2012) Metagenomic and metatranscriptomic analysis of microbial community structure and gene expression of activated sludge. PLoS ONE. doi:10.1371/journal.pone.0038183

    Google Scholar 

  • Zhang Y, Geng J, Ma H, Ren H, Xu K, Ding L (2016) Characterization of microbial community and antibiotic resistance genes in activated sludge under tetracycline and sulfamethoxazole selection pressure. Sci Total Environ 571:479–486

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are thankful to Council of Scientific and Industrial Research for providing necessary facilities and financial support to carry out this research. Ashwinkumar P. Rudrashetti is grateful to University Grant Commission (UGC), India for the award of a junior research fellowship. The manuscript represents communication number, CSIR-NEERI/KRC/2016/AUG/EBGD/3.

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Correspondence to R. A. Pandey.

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Rudrashetti, A.P., Jadeja, N.B., Gandhi, D. et al. Microbial population shift caused by sulfamethoxazole in engineered-Soil Aquifer Treatment (e-SAT) system. World J Microbiol Biotechnol 33, 121 (2017). https://doi.org/10.1007/s11274-017-2284-8

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