Skip to main content
SpringerLink
Log in

Characterization of the interactions between tetracycline antibiotics and microbial extracellular polymeric substances with spectroscopic approaches

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The antibiotics have attracted global attentions for their impact on aquatic ecosystem. The knowledge about the fate of antibiotics encountering extracellular polymeric substances (EPS) is, however, limited. In this study, we investigated the interacting mechanisms of tetracycline (TC) to EPS extracted from aerobic activated sludge. The contributions of the main components of EPS, extracellular proteins, and polysaccharides were evaluated using bovine serum albumin and alginate sodium, respectively. Fourier transform infrared spectroscopy, X-ray photoelectron spectroscopy, and nuclear magnetic resonance indicated that hydroxyl, carboxyl, and amino groups were the domain chemical groups involved in the interaction between TC and EPS, and the binding of TC onto EPS changed the structure of these chemical groups, thus causing shifts in their UV–visible absorption spectra. In addition, we found that extracellular proteins, rather than polysaccharides, were the major active contents involved in the interaction. Three-dimensional excitation–emission matrix fluorescence spectroscopy showed that the fluorophores in EPS were clearly quenched by TC and the static quenching process was observed, implying the complex formation of TC and EPS. Furthermore, thermodynamic analysis indicated that the binding of TC with EPS is spontaneous and dominated by electrostatic forces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anand U, Jash C, Boddepalli RK, Shrivastava A, Mukherjee S (2011) Exploring the mechanism of fluorescence quenching in proteins induced by tetracycline. J Phys Chem B 115:6312–6320

    Article  CAS  Google Scholar 

  • Caroni ALPF, de Lima CRM, Pereira MR, Fonseca JLC (2012) Tetracycline adsorption on chitosan: a mechanistic description based on mass uptake and zeta potential measurements. Colloids Surf B 100:222–228

    Article  CAS  Google Scholar 

  • Chen H, Luo HJ, Lan YC, Dong TT, Hu BJ, Wang YP (2011) Removal of tetracycline from aqueous solutions using polyvinylpyrrolidone (PVP-K30) modified nanoscale zero valent iron. J Hazard Mater 192:44–53

    CAS  Google Scholar 

  • Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710

    Article  CAS  Google Scholar 

  • Chen Y, Hu C, Qu JH, Yang M (2008) Photodegradation of tetracycline and formation of reactive oxygen species in aqueous tetracycline solution under simulated sunlight irradiation. J Photoch Photobio A 197:81–87

    Article  CAS  Google Scholar 

  • Chi ZX, Liu RT (2010) Phenotypic characterization of the binding of tetracycline to human serum albumin. Biomacromolecules 12:203–209

    Article  Google Scholar 

  • Chi ZX, Liu RT, Yang BJ, Zhang H (2010) Toxic interaction mechanism between oxytetracycline and bovine hemoglobin. J Hazard Mater 180:741–747

    Article  CAS  Google Scholar 

  • D'Abzac P, Bordas F, Joussein E, van Hullebusch E, Lens PL, Guibaud G (2012) Metal binding properties of extracellular polymeric substances extracted from anaerobic granular sludges. Environ Sci Pollut R 20(7):4509–4519

    Article  Google Scholar 

  • D'Abzac P, Bordas F, van Hullebusch E, Lens PNL, Guibaud G (2010) Effects of extraction procedures on metal binding properties of extracellular polymeric substances (EPS) from anaerobic granular sludges. Colloids Surf B 80:161–168

    Article  Google Scholar 

  • Dalmázio I, Almeida MO, Augusti R, Alves TMA (2007) Monitoring the degradation of tetracycline by ozone in aqueous medium via atmospheric pressure ionization mass spectrometry. J Am Soc Mass Spectrom 18:679–687

    Article  Google Scholar 

  • De Sousa FB, Oliveira MF, Lula IS, Sansiviero MTC, Cortés ME, Sinisterra RD (2008) Study of inclusion compound in solution involving tetracycline and β-cyclodextrin by FTIR-ATR. Vib Spectrosc 46:57–62

    Article  Google Scholar 

  • Delépée R, Maume D, Le Bizec B, Pouliquen H (2000) Preliminary assays to elucidate the structure of oxytetracycline's degradation products in sediments: determination of natural tetracyclines by high-performance liquid chromatography-fast atom bombardment mass spectrometry. J Chromatogr B 748:369–381

    Article  Google Scholar 

  • Erşan M, Bağda E, Bağda E (2013) Investigation of kinetic and thermodynamic characteristics of removal of tetracycline with sponge like, tannin based cryogels. Colloids Surf B 104:75–82

    Article  Google Scholar 

  • Fan CA, He JZ (2011) Proliferation of antibiotic resistance genes in microbial consortia of sequencing batch reactors (SBRs) upon exposure to trace erythromycin or erythromycin-H2O. Water Res 45:3098–3106

    Article  CAS  Google Scholar 

  • Frolund B, Palmgren R, Keiding K, Nielsen PH (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res 30:1749–1758

    Article  Google Scholar 

  • Gómez-Hortigüela L, López-Arbeloa F, Márquez-Álvarez C, Pérez-Pariente J (2013) Effect of fluorine and molecular charge-state on the aggregation behavior of (S)-(−)-N-benzylpyrrolidine-2-methanol confined within the AFI nanoporous structure. J Phys Chem C 117:8832–8839

    Article  Google Scholar 

  • Henriques IDS, Love NG (2007) The role of extracellular polymeric substances in the toxicity response of activated sludge bacteria to chemical toxins. Water Res 41:4177–4185

    Article  CAS  Google Scholar 

  • Her N, Amy G, McKnight D, Sohn J, Yoon Y (2003) Characterization of DOM as a function of MW by fluorescence EEM and HPLC-SEC using UVA, DOC, and fluorescence detection. Water Res 37:4295–4303

    Article  CAS  Google Scholar 

  • Herzberg M, Kang S, Elimelech M (2009) Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. Environ Sci Technol 43:4393–4398

    Article  CAS  Google Scholar 

  • Hu YJ, Liu Y, Zhao RM, Dong JX, Qu SS (2006) Spectroscopic studies on the interaction between methylene blue and bovine serum albumin. J Photoch Photobio A 179:324–329

    Article  CAS  Google Scholar 

  • Jia SR, Yu HF, Lin YX, Dai YJ (2007) Characterization of extracellular polysaccharides from Nostoc flagelliforme cells in liquid suspension culture. Biotechnol and Bioproc E 12:271–275

    Article  CAS  Google Scholar 

  • Jiao SJ, Zheng SR, Yin DQ, Wang LH, Chen LY (2008) Aqueous photolysis of tetracycline and toxicity of photolytic products to luminescent bacteria. Chemosphere 73:377–382

    Article  CAS  Google Scholar 

  • Khunjar WO, Mackintosh SA, Skotnicka Pitak J, Baik S, Aga DS, Love NG (2011) Elucidating the relative roles of ammonia oxidizing and heterotrophic bacteria during the biotransformation of 17α-ethinylestradiol and trimethoprim. Environ Sci Technol 45:3605–3612

    Article  CAS  Google Scholar 

  • Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473

    Article  CAS  Google Scholar 

  • Liu RT, Sun F, Zhang LJ, Zong WS, Zhao XC, Wang L, Wu RL, Hao XP (2009) Evaluation on the toxicity of nanoAg to bovine serum albumin. Sci Total Environ 407:4184–4188

    Article  CAS  Google Scholar 

  • Loewus FA (1952) Improvement in anthrone method for determination of carbohydrates. Anal Chem 24:219–219

    Article  CAS  Google Scholar 

  • Lu R, Sheng GP, Liang Y, Li WH, Tong ZH, Chen W, Yu HQ (2013) Characterizing the interactions between polycyclic aromatic hydrocarbons and fulvic acids in water. Environ Sci Pollut R 20:2220–2225

    Article  CAS  Google Scholar 

  • Métivier R, Bourven I, Labanowski J, Guibaud G (2013) Interaction of erythromycin ethylsuccinate and acetaminophen with protein fraction of extracellular polymeric substances (EPS) from various bacterial aggregates. Environ Sci Pollut R:1–11. doi:10.1007/s11356-013-1738-2

  • Mandal G, Bhattacharya S, Ganguly T (2009) Investigations to reveal the nature of interactions between bovine hemoglobin and semiconductor zinc oxide nanoparticles by using various optical techniques. Chem Phys Lett 478:271–276

    Article  CAS  Google Scholar 

  • Omoike A, Chorover J (2004) Spectroscopic study of extracellular polymeric substances from Bacillus subtilis: aqueous chemistry and adsorption effects. Biomacromolecules 5:1219–1230

    Article  CAS  Google Scholar 

  • Ozturk S, Aslim B (2008) Relationship between chromium(VI) resistance and extracellular polymeric substances (EPS) concentration by some cyanobacterial isolates. Environ Sci Pollut R 15:478–480

    Article  CAS  Google Scholar 

  • Pan XL, Liu J, Zhang DY (2010a) Binding of phenanthrene to extracellular polymeric substances (EPS) from aerobic activated sludge: a fluorescence study. Colloids Surf B 80:103–106

    Article  CAS  Google Scholar 

  • Pan XR, Liu RT, Qin PF, Wang L, Zhao XC (2010b) Spectroscopic studies on the interaction of acid yellow with bovine serum albumin. J Lumin 130:611–617

    Article  CAS  Google Scholar 

  • Perez S, Eichhorn P, Aga DS (2005) Evaluating the biodegradability of sulfamethazine, sulfamethoxazole, sulfathiazole, and trimethoprim at different stages of sewage treatment. Environ Toxicol Chem 24:1361–1367

    Article  CAS  Google Scholar 

  • Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  Google Scholar 

  • Schlunzen F, Zarivach R, Harms J, Bashan A, Tocilj A, Albrecht R, Yonath A, Franceschi F (2001) Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413:814–821

    Article  CAS  Google Scholar 

  • Sheng GP, Yu HQ (2006) Characterization of extracellular polymeric substances of aerobic and anaerobic sludge using three-dimensional excitation and emission matrix fluorescence spectroscopy. Water Res 40:1233–1239

    Article  CAS  Google Scholar 

  • Sheng GP, Zhang ML, Yu HQ (2008) Characterization of adsorption properties of extracellular polymeric substances (EPS) extracted from sludge. Colloids Surf B 62:83–90

    Article  CAS  Google Scholar 

  • Shi YJ, Wang XH, Yu HB, Xie HJ, Teng SX, Sun XF, Tian BH, Wang SG (2011) Aerobic granulation for nitrogen removal via nitrite in a sequencing batch reactor and the emission of nitrous oxide. Bioresource Technol 102:2536–2541

    Article  CAS  Google Scholar 

  • Sponza DT, Çelebi H (2012) Removal of oxytetracycline (OTC) in a synthetic pharmaceutical wastewater by a sequential anaerobic multichamber bed reactor (AMCBR)/completely stirred tank reactor (CSTR) system: biodegradation and inhibition kinetics. Bioresource Technol 104:100–110

    Article  CAS  Google Scholar 

  • Su KZ, Yu HQ (2005) Formation and characterization of aerobic granules in a sequencing batch reactor treating soybean-processing wastewater. Environ Sci Technol 39:2818–2827

    Article  CAS  Google Scholar 

  • Sun XF, Wang SG, Cheng W, Fan MH, Tian BH, Gao BY, Li XM (2011) Enhancement of acidic dye biosorption capacity on poly(ethylenimine) grafted anaerobic granular sludge. J Hazard Mater 189:27–33

    Article  CAS  Google Scholar 

  • Sun XF, Wang SG, Zhang XM, Paul Chen J, Li XM, Gao BY, Ma Y (2009) Spectroscopic study of Zn2+ and Co2+ binding to extracellular polymeric substances (EPS) from aerobic granules. J Colloid Interface Sci 335:11–17

    Article  CAS  Google Scholar 

  • Tian FF, Jiang FL, Han XL, Xiang C, Ge YS, Li JH, Zhang Y, Li R, Ding XL, Liu Y (2010) Synthesis of a novel hydrazone derivative and biophysical studies of its interactions with bovine serum albumin by spectroscopic, electrochemical, and molecular docking methods. J Phys Chem B 114:14842–14853

    Article  CAS  Google Scholar 

  • Wang GK, Wang DC, Li X, Lu Y (2011a) Exploring the binding mechanism of dihydropyrimidinones to human serum albumin: spectroscopic and molecular modeling techniques. Colloids Surf B 84:272–279

    Article  CAS  Google Scholar 

  • Wang LL, Wang LF, Ren XM, Ye XD, Li WW, Yuan SJ, Sun M, Sheng GP, Yu HQ, Wang XK (2011b) pH dependence of structure and surface properties of microbial EPS. Environ Sci Technol 46:737–744

    Article  Google Scholar 

  • Wang ZK, Hessler CM, Xue Z, Seo Y (2012) The role of extracellular polymeric substances on the sorption of natural organic matter. Water Res 46:1052–1060

    Article  CAS  Google Scholar 

  • Wu TQ, Guan SY, Su HX, Cai ZJ, Wu Q (2007) Binding of the environmental pollutant naphthol to bovine serum albumin. Biomacromolecules 8:1899–1906

    Article  CAS  Google Scholar 

  • Xu J, Sheng GP, Ma Y, Wang LF, Yu HQ (2013) Roles of extracellular polymeric substances (EPS) in the migration and removal of sulfamethazine in activated sludge system. Water Res. doi:10.1016/j.watres.2013.06.009

  • Yang QQ, Liang JG, Han HY (2009) Probing the interaction of magnetic iron oxide nanoparticles with bovine serum albumin by spectroscopic techniques. J Phys Chem B 113:10454–10458

    Article  CAS  Google Scholar 

  • Yang SF, Lin CF, Wu CJ, Ng K, Lin YC, Angela, Andy Hong PK (2012) Fate of sulfonamide antibiotics in contact with activated sludge-sorption and biodegradation. Water Res 46:1301–1308

    Article  CAS  Google Scholar 

  • Yuan SJ, Sun M, Sheng GP, Li Y, Li WW, Yao RS, Yu HQ (2010) Identification of key constituents and structure of the extracellular polymeric substances excreted by Bacillus megaterium TF10 for their flocculation capacity. Environ Sci Technol 45:1152–1157

    Article  Google Scholar 

  • Zhang HX, Huang X, Zhang M (2008) Thermodynamic studies on the interaction of dioxopromethazine to β-cyclodextrin and bovine serum albumin. J Fluoresc 18:753–760

    Article  CAS  Google Scholar 

  • Zhang SJ, Jiang YL, Chen CS, Spurgin J, Schwehr KA, Quigg A, Chin WC, Santschi PH (2012) Aggregation, dissolution, and stability of quantum dots in marine environments: importance of extracellular polymeric substances. Environ Sci Technol 46:8764–8772

    Article  CAS  Google Scholar 

  • Zhao LZ, Liu RT, Zhao XC, Yang BJ, Gao CZ, Hao XP, Wu YZ (2009) New strategy for the evaluation of CdTe quantum dot toxicity targeted to bovine serum albumin. Sci Total Environ 407:5019–5023

    Article  CAS  Google Scholar 

  • Zhao XC, Liu RT, Teng Y, Liu XF (2011) The interaction between Ag+ and bovine serum albumin: a spectroscopic investigation. Sci Total Environ 409:892–897

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Program for New Century Excellent Talents in University (NCET-10-0528) and the National Natural Science Foundation of China (51178254). The authors wish to thank the Natural Science Foundation of Shandong Province (2009ZRB01618), Natural Science Foundation for Distinguished Young Scholars of Shandong Province (JQ201116), and the Independent Innovation Foundation of Shandong University (2011GN044) for the support of this work.

Author information

Authors and Affiliations

  1. Shandong Key Laboratory of Water Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Shandong University, Jinan, 250100, China

    Chao Song, Xue-Fei Sun, Su-Fang Xing, Peng-Fei Xia, Yi-Jing Shi & Shu-Guang Wang

Authors
  1. Chao Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue-Fei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Su-Fang Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peng-Fei Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi-Jing Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shu-Guang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xue-Fei Sun or Shu-Guang Wang.

Additional information

Responsible editor: Hongwen Sun

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 1,618 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, C., Sun, XF., Xing, SF. et al. Characterization of the interactions between tetracycline antibiotics and microbial extracellular polymeric substances with spectroscopic approaches. Environ Sci Pollut Res 21, 1786–1795 (2014). https://doi.org/10.1007/s11356-013-2070-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2070-6

Keywords

Search

Navigation