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Degradation of oxytetracycline and its impacts on biogas-producing microbial community structure

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Abstract

The effect of veterinary antibiotics in anaerobic digesters is a concern where methane production efficiency is highly dependent on microbial community structure. In this study, both anaerobic degradation of a common veterinary antibiotic, oxytetracycline (OTC), and its effects on an anaerobic digester microbial community were investigated. Qualitative and quantitative molecular tools were used to monitor changes in microbial community structure during a 60-day batch incubation period of cow manure with the addition of different concentrations of the antibiotic. Molecular data were interpreted by a further redundancy analysis as a multivariate statistics approach. At the end of the experiment, approximately 48, 33, and 17 % of the initially added 50, 100, and 200 mg l−1 of OTC was still present in the serum bottles which reduced the biogas production via accumulation of some of the volatile fatty acids (VFAs). Biogas production was highly correlated with Methanobacteriales and Methanosarcinales gene copy numbers, and those parameters were negatively affected with oxytetracycline and VFA concentrations.

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References

  1. 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):1637–1643. doi:10.1016/j.procbio.2006.03.010

    Article  CAS  Google Scholar 

  2. De Liguoro M, Cibin V, Capolongo F, Halling-Sørensen B, Montesissa C (2003) Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere 52(1):203–212. doi:10.1016/s0045-6535(03)00284-4

    Article  Google Scholar 

  3. Ince B, Coban H, Turker G, Ertekin E, Ince O (2013) Effect of oxytetracycline on biogas production and active microbial populations during batch anaerobic digestion of cow manure. Bioprocess Biosyst Eng 36(5):541–546

    Article  CAS  Google Scholar 

  4. Beneragama N, Lateef SA, Iwasaki M, Yamashiro T, Umetsu K (2013) The combined effect of cefazolin and oxytertracycline on biogas production from thermophilic anaerobic digestion of dairy manure. Bioresour Technol 133:23–30

    Article  CAS  Google Scholar 

  5. Ke X, Wang C, Li R (2014) Effects of oxytetracycline on methane production and the microbial communities during anaerobic digestion of cow manure. J Integr Agric 6(13):1373–1381

    Article  Google Scholar 

  6. Akyol Ç, Ince O, Cetecioglu Z, Ustun Alkan F, Ince B (2015) The fate of oxytetracycline in two-phase and single-phase anaerobic cattle manure digesters and its effects on microbial communities. J Chem Technol Biotechnol 91(3):806–814

    Article  Google Scholar 

  7. Ahring BK, Sandberg M, Angelidaki I (1995) Volatile fatty acids as indicators of process imbalance in anaerobic digestors. Appl Microbiol Biotechnol 43(3):559–565

    Article  CAS  Google Scholar 

  8. Massé DI, Lu D, Masse L, Droste RL (2000) Effect of antibiotics on psychrophilic anaerobic digestion of swine manure slurry in sequencing batch reactors. Bioresour Technol 75(3):205–211. doi:10.1016/s0960-8524(00)00046-8

    Article  Google Scholar 

  9. Aydin S, Cetecioglu Z, Arikan O, Ince B, Ozbayram EG, Ince O (2015) Inhibitory effects of antibiotic combinations on syntrophic bacteria, homoacetogens and methanogens. Chemosphere 120:515–520. doi:10.1016/j.chemosphere.2014.09.045

    Article  CAS  Google Scholar 

  10. Poulsen LK, Ballard G, Stahl DA (1993) Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl Environ Microbiol 59(5):1354–1360

    CAS  Google Scholar 

  11. Moter A, Göbel UB (2000) Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms. J Microbiol Methods 41(2):85–112. doi:10.1016/S0167-7012(00)00152-4

    Article  CAS  Google Scholar 

  12. Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166(2):145–167. doi:10.1002/jpln.200390023

    Article  CAS  Google Scholar 

  13. Cetecioglu Z, Ince B, Azman S, Ince O (2014) Biodegradation of tetracycline under various conditions and effects on microbial community. Appl Biochem Biotechnol 172(2):631–640. doi:10.1007/s12010-013-0559-6

    Article  CAS  Google Scholar 

  14. APHA (2005) Standard methods for the examination of water and wastewater, 21 edn. APHA, Washington, DC

  15. Yuan S, Wang Q, Yates SR, Peterson NG (2010) Development of an efficient extraction method for oxytetracycline in animal manure for high performance liquid chromatography analysis. J Environ Sci Health Part B 45(7):612–620. doi:10.1080/03601234.2010.502404

    Article  CAS  Google Scholar 

  16. Ovreas L, Forney L, Daae F, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63(9):3367–3373

    CAS  Google Scholar 

  17. Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60(4):1232–1240

    CAS  Google Scholar 

  18. Shinzato N, Matsumoto T, Yamaoka I, Oshima T, Yamagishi A (1999) Phylogenetic diversity of symbiotic methanogens living in the hindgut of the lower termite Reticulitermes speratus analyzed by PCR and in situ hybridization. Appl Environ Microbiol 65(2):837–840

    CAS  Google Scholar 

  19. Lane DJ (1991) 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

  20. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700

    CAS  Google Scholar 

  21. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89(6):670–679. doi:10.1002/bit.20347

    Article  CAS  Google Scholar 

  22. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    CAS  Google Scholar 

  23. Álvarez JA, Otero L, Lema JM, Omil F (2010) The effect and fate of antibiotics during the anaerobic digestion of pig manure. Bioresour Technol 101(22):8581–8586. doi:10.1016/j.biortech.2010.06.075

    Article  Google Scholar 

  24. Wang Q, Yates SR (2008) Laboratory study of oxytetracycline degradation kinetics in animal manure and soil. J Agric Food Chem 56(5):1683–1688

    Article  CAS  Google Scholar 

  25. Loke M-L, Jespersen S, Vreeken R, Halling-Sørensen B, Tjørnelund J (2003) Determination of oxytetracycline and its degradation products by high-performance liquid chromatography–tandem mass spectrometry in manure-containing anaerobic test systems. J Chromatogr B 783(1):11–23. doi:10.1016/s1570-0232(02)00468-3

    Article  Google Scholar 

  26. Turker G, Ince O, Ertekin E, Akyol C, Ince B (2013) Changes in performance and active microbial communities due to single and multiple effects of mixing and solid content in anaerobic digestion process of OTC medicated cattle manure. Int J Renew Energy Res (IJRER) 3(1):144–148

    Google Scholar 

  27. Schnappinger D, Hillen W (1996) Tetracyclines: antibiotic action, uptake, and resistance mechanisms. Arch Microbiol 165(6):359–369

    Article  CAS  Google Scholar 

  28. Garcia-Peña E, Parameswaran P, Kang D, Canul-Chan M, Krajmalnik-Brown R (2011) Anaerobic digestion and co-digestion processes of vegetable and fruit residues: process and microbial ecology. Bioresour Technol 102(20):9447–9455

    Article  Google Scholar 

  29. Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehöver P, Pühler A (2009) Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. J Biotechnol 142(1):38–49

    Article  Google Scholar 

  30. Lindh JM, Terenius O, Faye I (2005) 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 71(11):7217–7223

    Article  CAS  Google Scholar 

  31. La Duc MT, Nicholson W, Kern R, Venkateswaran K (2003) Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ Microbiol 5(10):977–985

    Article  Google Scholar 

  32. Li A, Yn Chu, Wang X, Ren L, Yu J, Liu X, Yan J, Zhang L, Wu S, Li S (2013) A pyrosequencing-based metagenomic study of methane-producing microbial community in solid-state biogas reactor. Biotechnol Biofuels 6(3):1–17

    CAS  Google Scholar 

  33. Ferry JG (1993) Fermentation of acetate. In: Methanogenesis. Springer, New York, pp 304–334

  34. Zinder SH, Koch M (1984) Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch Microbiol 138(3):263–272

    Article  CAS  Google Scholar 

  35. Karakashev D, Batstone DJ, Trably E, Angelidaki I (2006) Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Appl Environ Microbiol 72(7):5138–5141. doi:10.1128/aem.00489-06

    Article  CAS  Google Scholar 

  36. Schnurer A, Nordberg A (2008) Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature. Wat Sci Tech 57(5):735–740

    Article  CAS  Google Scholar 

  37. Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Biotechnol 7(2):173–190. doi:10.1007/s11157-008-9131-1

    Article  CAS  Google Scholar 

  38. Stone JJ, Clay SA, Zhu Z, Wong KL, Porath LR, Spellman GM (2009) Effect of antimicrobial compounds tylosin and chlortetracycline during batch anaerobic swine manure digestion. Water Res 43(18):4740–4750. doi:10.1016/j.watres.2009.08.005

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We appreciate the grants from the Scientific and Technical Research Council of Turkey (TUBITAK, Project No: 109Y275). The authors are grateful to the Pharmacology and Toxicology Department of Istanbul University, Faculty of Veterinary Medicine for providing cow manure, A. M. Detweiler and L. M. Tom for English proofreading, and two anonymous reviewers for improving the scientific quality of the manuscript.

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    Authors and Affiliations

    1. Institute of Environmental Sciences, Bogazici University, Bebek, 34342, Istanbul, Turkey

      Halil Coban, Emine Ertekin, Gokhan Turker, Çağrı Akyol & Bahar Ince

    2. Department of Environmental Engineering, Istanbul Technical University, Maslak, 34469, Istanbul, Turkey

      Orhan Ince

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    1. Halil Coban
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    Correspondence to Halil Coban.

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    H. Coban and E. Ertekin contributed equally to this work.

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    Coban, H., Ertekin, E., Ince, O. et al. Degradation of oxytetracycline and its impacts on biogas-producing microbial community structure. Bioprocess Biosyst Eng 39, 1051–1060 (2016). https://doi.org/10.1007/s00449-016-1583-z

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    • DOI: https://doi.org/10.1007/s00449-016-1583-z

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