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Applied Microbiology and Biotechnology

, Volume 100, Issue 5, pp 2417–2427 | Cite as

Long-term effects of heavy metals and antibiotics on granule-based anammox process: granule property and performance evolution

  • Zheng-Zhe Zhang
  • Qian-Qian Zhang
  • Jia-Jia Xu
  • Zhi-Jian Shi
  • Qiong Guo
  • Xiao-Yan Jiang
  • Hui-Zhong Wang
  • Guo-He Chen
  • Ren-Cun JinEmail author
Environmental biotechnology

Abstract

The feasibility of the anaerobic ammonium oxidation (anammox) process to treat synthetic swine wastewater containing antibiotics and heavy metals was studied in this work. Nitrogen removal performance and granule characteristics were tracked by continuous-flow monitoring to evaluate the long-term joint effects of Cu and Zn and of Cu and oxytetracycline (OTC). Cu and Zn with a joint loading rate (JLR) of 0.04 kg m−3 day−1 did not affect the performance, while a JLR of 0.12 kg m−3 day−1 caused a rapid collapse in performance. Cu and OTC addition with a JLR of 0.04 kg m−3 day−1 for approximately 2 weeks induced significant nitrite accumulation. Granule characteristic analysis elucidated the disparate inhibition mechanisms of heavy metals and antibiotics: the internalization of heavy metals caused metabolic disorders, whereas OTC functioned as a growth retarder. However, anammox reactors could adapt to a JLR of 0.04 kg m−3 day−1 via self-regulation during the acclimatization to subinhibitory concentrations, which had a stable nitrogen removal rate (>8.5 kg m−3 day−1) and removal rate efficiency (>75 %) for reactors with Cu-OTC addition. Therefore, this study supports the great potential of using anammox granules to treat swine wastewater.

Keywords

Anammox Swine wastewater Heavy metal inhibition Antibiotic inhibition Sludge characteristics 

Notes

Acknowledgments

The authors wish to thank the National Key Technologies R&D Program of China (No. 2012BAC13B02), the Public Welfare Project of Science Technology Department of Zhejiang Province, the Xinmiao Talent Program of Zhejiang Province (No. 2015R423074), and the Xingguang Program of Hangzhou Normal University for their partial support of this study.

Compliance with ethical standards

Funding

This study was funded by the National Key Technologies R&D Program of China (No. 2012BAC13B02), the Public Welfare Project of Science Technology Department of Zhejiang Province, the Xinmiao Talent Program of Zhejiang Province (No. 2015R423074), and the Xingguang Program of Hangzhou Normal University.

Conflict of interest

The corresponding author on behalf of all authors of the paper declares no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2015_7120_MOESM1_ESM.pdf (38 kb)
ESM 1 (PDF 38 kb)

References

  1. APHA, AWWA, AEF (2005) Standard methods for the examination of water and wastewater, 21st edn. Washington, DC, USA, American Public Health AssociationGoogle Scholar
  2. Arikan OA, Sikora LJ, Mulbry W, Khan SU, Rice C, Foster GD (2006) The fate and effect of oxytetracycline during the anaerobic digestion of manure from therapeutically treated calves. Process Biochem 41(7):1637–1643CrossRefGoogle Scholar
  3. Ben W, Qiang Z, Pan X, Chen M (2009) Removal of veterinary antibiotics from sequencing batch reactor (SBR) pretreated swine wastewater by Fenton’s reagent. Water Res 43(17):4392–4402CrossRefPubMedGoogle Scholar
  4. Carvajal-Arroyo JM, Puyol D, Li G, Swartwout A, Sierra-Álvarez R, Field JA (2014) Starved anammox cells are less resistant to NO2 inhibition. Water Res 65:170–176CrossRefPubMedGoogle Scholar
  5. Chen H, Yu J, Jia X, Jin R (2014) Enhancement of anammox performance by Cu(II), Ni(II) and Fe(III) supplementation. Chemosphere 117:610–616CrossRefPubMedGoogle Scholar
  6. Cloete TE (2003) Resistance mechanisms of bacteria to antimicrobial compounds. Int Biodeter Biodegrad 51(4):277–282CrossRefGoogle Scholar
  7. Gu C, Karthikeyan KG, Sibley SD, Pedersen JA (2007) Complexation of the antibiotic tetracycline with humic acid. Chemosphere 66(8):1494–1501CrossRefPubMedGoogle Scholar
  8. Hu Z, Chandran K, Grasso D, Smets BF (2003) Impact of metal sorption and internalization on nitrification inhibition. Environ. Sci. Technol 37(4):728–734CrossRefPubMedGoogle Scholar
  9. Hu Z, van Alen T, Jetten MSM, Kartal B (2013) Lysozyme and penicillin inhibit the growth of anaerobic ammonium-oxidizing planctomycetes. Appl Environ Microb 79(24):7763–7769CrossRefGoogle Scholar
  10. Jetten MS, Niftrik LV, Strous M, Kartal B, Keltjens JT, Op Den Camp HJ (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol 44(2–3):65–84CrossRefGoogle Scholar
  11. Jin H, Chang Z (2011) Distribution of heavy metal contents and chemical fractions in anaerobically digested manure slurry. Appl Biochem Biotech 164(3):268–282CrossRefGoogle Scholar
  12. Jin R, Zhang Q, Zhang Z, Liu J, Yang B, Guo L, Wang H (2014) Bio-augmentation for mitigating the impact of transient oxytetracycline shock on anaerobic ammonium oxidation (ANAMMOX) performance. Bioresour Technol 163:244–253CrossRefPubMedGoogle Scholar
  13. Kimura Y, Isaka K (2014) Evaluation of inhibitory effects of heavy metals on anaerobic ammonium oxidation (anammox) by continuous feeding tests. Appl Microbiol Biot 98(16):6965–6972CrossRefGoogle Scholar
  14. Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303CrossRefPubMedGoogle Scholar
  15. Lee S, Maken S, Jang J, Park K, Park J (2006) Development of physicochemical nitrogen removal process for high strength industrial wastewater. Water Res 40(5):975–980CrossRefPubMedGoogle Scholar
  16. Liu H, Fang HHP (2002) Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol Bioeng 80(7):806–811CrossRefPubMedGoogle Scholar
  17. Liu Y, Ni B (2015) Appropriate Fe (II) addition significantly enhances anaerobic ammonium oxidation (anammox) activity through improving the bacterial growth rate. Sci Rep 5:8204PubMedCentralCrossRefPubMedGoogle Scholar
  18. Lotti T, Cordola M, Kleerebezem R, Caffaz S, Lubello C, van Loosdrecht M (2012) Inhibition effect of swine wastewater heavy metals and antibiotics on anammox activity. Water Sci Technol 66(7):1519–1526CrossRefPubMedGoogle Scholar
  19. Luis Campos J, Garrido J, Méndez R, Lema J (2001) Effect of two broad-spectrum antibiotics on activity and stability of continuous nitrifying system. Appl Biochem Biotech 95(1):1–10CrossRefGoogle Scholar
  20. Mei X, Wang Z, Zheng X, Huang F, Ma J, Tang J, Wu Z (2014) Soluble microbial products in membrane bioreactors in the presence of ZnO nanoparticles. J Membrane Sci 451:169–176CrossRefGoogle Scholar
  21. Ochoa-Herrera V, León G, Banihani Q, Field JA, Sierra-Alvarez R (2011) Toxicity of copper(II) ions to microorganisms in biological wastewater treatment systems. Sci Total Environ 412-413:380–385CrossRefPubMedGoogle Scholar
  22. Strous M, Heijnen JJ, Kuenen JG, Jetten M (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50(5):589–596CrossRefGoogle Scholar
  23. Suzuki K, Waki M, Yasuda T, Fukumoto Y, Kuroda K, Sakai T, Suzuki N, Suzuki R, Matsuba K (2010) Distribution of phosphorus, copper and zinc in activated sludge treatment process of swine wastewater. Bioresour Technol 101(23):9399–9404CrossRefPubMedGoogle Scholar
  24. Tang C, Zheng P, Chen T, Zhang J, Mahmood Q, Ding S, Chen X, Chen J, Wu D (2011a) Enhanced nitrogen removal from pharmaceutical wastewater using SBA-ANAMMOX process. Water Res 45(1):201–210CrossRefPubMedGoogle Scholar
  25. Tang C, Zheng P, Wang C, Mahmood Q, Zhang J, Chen X, Zhang L, Chen J (2011b) Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res 45(1):135–144CrossRefPubMedGoogle Scholar
  26. Vanotti MB, Szogi AA, Hunt PG, Millner PD, Humenik FJ (2007) Development of environmentally superior treatment system to replace anaerobic swine lagoons in the USA. Bioresour Technol 98(17):3184–3194CrossRefPubMedGoogle Scholar
  27. Wu J, Zhou H, Li H, Zhang P, Jiang J (2009) Impacts of hydrodynamic shear force on nucleation of flocculent sludge in anaerobic reactor. Water Res 43(12):3029–3036CrossRefPubMedGoogle Scholar
  28. Yamamoto T, Takaki K, Koyama T, Furukawa K (2008) Long-term stability of partial nitritation of swine wastewater digester liquor and its subsequent treatment by anammox. Bioresour Technol 99(14):6419–6425CrossRefPubMedGoogle Scholar
  29. Yang G, Jin R (2012) The joint inhibitory effects of phenol, copper (II), oxytetracycline (OTC) and sulfide on anammox activity. Bioresour Technol 126:187–192CrossRefPubMedGoogle Scholar
  30. Yin C, Meng F, Chen G (2015) Spectroscopic characterization of extracellular polymeric substances from a mixed culture dominated by ammonia-oxidizing bacteria. Water Res 68:740–749CrossRefPubMedGoogle Scholar
  31. Zhang Q, Chen H, Liu J, Yang B, Ni W, Jin R (2014) The robustness of ANAMMOX process under the transient oxytetracycline (OTC) shock. Bioresour Technol 153:39–46CrossRefPubMedGoogle Scholar
  32. Zhang Q, Zhang Z, Guo Q, Wang J, Wang H, Jin R (2015b) Analyzing the revolution of anaerobic ammonium oxidation (anammox) performance and sludge characteristics under zinc inhibition. Appl Microbiol Biot 99(7):3221–3232CrossRefGoogle Scholar
  33. Zhang Q, Zhang Z, Guo Q, Chen Q, Jin R, Jia X (2015c) Variation in the performance and sludge characteristics of anaerobic ammonium oxidation inhibited by copper. Sep Purif Technol 142:108–115CrossRefGoogle Scholar
  34. Zhang Z, Zhang Q, Guo Q, Chen Q, Jiang X, Jin R (2015a) Anaerobic ammonium-oxidizing bacteria gain antibiotic resistance during long-term acclimatization. Bioresour Technol 192:756–764CrossRefPubMedGoogle Scholar
  35. Zhang Z, Cheng Y, Zhou Y, Buayi X, Jin R (2015d) A novel strategy for accelerating the recovery of an anammox reactor inhibited by copper(II): EDTA washing combined with biostimulation via low-intensity ultrasound. Chem Eng J 279:912–920CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Zheng-Zhe Zhang
    • 1
    • 2
  • Qian-Qian Zhang
    • 1
    • 2
  • Jia-Jia Xu
    • 1
    • 2
  • Zhi-Jian Shi
    • 1
    • 2
  • Qiong Guo
    • 1
    • 2
  • Xiao-Yan Jiang
    • 1
    • 2
  • Hui-Zhong Wang
    • 1
  • Guo-He Chen
    • 3
  • Ren-Cun Jin
    • 1
    • 2
    Email author
  1. 1.College of Life and Environmental SciencesHangzhou Normal UniversityHangzhouChina
  2. 2.Key Laboratory of Hangzhou City for Ecosystem Protection and RestorationHangzhou Normal UniversityHangzhouChina
  3. 3.College of Life SciencesShaoxing UniversityShaoxingChina

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