Abstract
The antibiotic tiamulin (TIA) is common and widely used medication for dysentery eradication in swine productions. Tiamulin persists in livestock manure, and its residues have been found in various environment. This work obtained four tiamulin-degrading enriched bacterial consortia from a covered anaerobic lagoon system and a stabilized pond system of swine farms. Tiamulin was efficiently removed by the enriched cultures at the concentrations between 2.5 and 200 mg/L, with a removal of 60.1–99.9% during 16 h and a degradation half-life of 4.5–15.7 h. The stabilized pond system cultured with taimulin solely could eliminate tiamulin at the highest rates. The logistic substrate degradation model fit most of the experimental data. Next-generation amplicon sequencing was conducted, and it was found that the bacterial community was significantly impacted by the inoculum source, nutrient addition, and high tiamulin concentrations. Principal coordinate analysis (PCoA) indicated the similarity of bacterial communities in the original enriched samples and the 2.5 mg/L tiamulin-removed cultures. The 200 mg/L consortia were rather different and became similar to the other 200 mg/L consortia from different sources and cultures without nutrient supplementation. Shannon and Simpson indices suggested a reduction in bacterial diversity at high concentrations. The microbes that had high growth in the most efficient enriched culture, or which were abundant in all samples, or which increased with higher tiamulin concentrations were likely to be the major tiamulin-degrading bacteria. This is the first report suggested the possible roles of Achromobacter, Delftia, Flavobacterium, Pseudomonas, and Stenotrophomonas in tiamulin degradation.
Similar content being viewed by others
References
Aalipour F, Mirlohi M, Jalali M. Determination of antibiotic consumption index for animal originated foods produced in animal husbandry in Iran, 2010. J Environ Health Sci Eng. 2014;12(1):42. https://doi.org/10.1186/2052-336x-12-42.
Sarmah AK, Meyer MT, Boxall AB. A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere. 2006;65(5):725–59. https://doi.org/10.1016/j.chemosphere.2006.03.026.
An NQ. Using antibiotics in animal husbandry in Vietnam (in Vietnam). 2012. http://nhanloc.net/ Accessed 22/1/2019.
Schlüsener MP, Spiteller M, Bester K. Determination of antibiotics from soil by pressurized liquid extraction and liquid chromatography–tandem mass spectrometry. J Chromatogr A. 2003;1003(1):21–8. https://doi.org/10.1016/S0021-9673(03)00737-4.
Ben W, Qiang Z, Adams C, Zhang H, Chen L. Simultaneous determination of sulfonamides, tetracyclines and tiamulin in swine wastewater by solid-phase extraction and liquid chromatography-mass spectrometry. J Chromatogr A. 2008;1202(2):173–80. https://doi.org/10.1016/j.chroma.2008.07.014.
Ben W, Pan X, Qiang Z. Occurrence and partition of antibiotics in the liquid and solid phases of swine wastewater from concentrated animal feeding operations in Shandong Province, China. Environ Sci Processes & Impacts. 2013;15(4):870–5. https://doi.org/10.1039/C3EM30845F.
Bartelt-Hunt S, Snow DD, Damon-Powell T, Miesbach D. Occurrence of steroid hormones and antibiotics in shallow groundwater impacted by livestock waste control facilities. J Contam Hydrol. 2011;123(3–4):94–103. https://doi.org/10.1016/j.jconhyd.2010.12.010.
Lin T, Yu S, Chen W. Occurrence, removal and risk assessment of pharmaceutical and personal care products (PPCPs) in an advanced drinking water treatment plant (ADWTP) around Taihu Lake in China. Chemosphere. 2016;152:1–9. https://doi.org/10.1016/j.chemosphere.2016.02.109.
Qiao T, Yu Z, Zhang X, Au DWT. Occurrence and fate of pharmaceuticals and personal care products in drinking water in southern China. J Environ Monit. 2011;13(11):3097–103. https://doi.org/10.1039/C1EM10318K.
Wang Z, Zhang X-H, Huang Y, Wang H. Comprehensive evaluation of pharmaceuticals and personal care products (PPCPs) in typical highly urbanized regions across China. Environ Pollut. 2015;204:223–32. https://doi.org/10.1016/j.envpol.2015.04.021.
Bosevski I, Zgajnar Gotvajn A. Ozonation as a cost effective technology in antimicrobial resistance management of wastewater and sludge. In: 15th International Conference on Environmental Science and Technology; 31 August to 2 September 2017; Rhodes, Greece 2017
Schlusener MP, Bester K. Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environ Pollut. 2006;143(3):565–71. https://doi.org/10.1016/j.envpol.2005.10.049.
Schlusener MP, von Arb MA, Bester K. Elimination of macrolides, tiamulin, and salinomycin during manure storage. Arch Environ Contam Toxicol. 2006;51(1):21–8. https://doi.org/10.1007/s00244-004-0240-8.
Nguyen TKX, Thayanukul P, Pinyakong O, Suttinun O. Tiamulin removal by wood-rot fungi isolated from swine farms and role of ligninolytic enzymes. Int Biodeterior Biodegradation. 2017;116:147–54. https://doi.org/10.1016/j.ibiod.2016.10.010.
Simkins S, Alexander M. Models for mineralization kinetics with the variables of substrate concentration and population density. Appl Environ Microbiol. 1984;47(6):1299–306.
Cancho Grande B, García Falcón MS, Pérez-Lamela C, Rodríguez Comesaña M, Simal GJ. Quantitative analysis of colistin and tiamulin in liquid and solid medicated premixes by HPLC with diode-array detection. Chromatographia. 2001;53(1):S460–S3. https://doi.org/10.1007/bf02490378.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6. https://doi.org/10.1038/nmeth.f.303 https://www.nature.com/articles/nmeth.f.303#supplementary-information.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England). 2011;27(16):2194–200. https://doi.org/10.1093/bioinformatics/btr381.
Chao A, Chazdon RL, Colwell RK, Shen T-J. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett. 2005;8(2):148–59. https://doi.org/10.1111/j.1461-0248.2004.00707.x.
Rodrigues VD, Torres TT, Ottoboni LMM. Bacterial diversity assessment in soil of an active Brazilian copper mine using high-throughput sequencing of 16S rDNA amplicons. Antonie Van Leeuwenhoek. 2014;106(5):879–90. https://doi.org/10.1007/s10482-014-0257-6.
Simpson EH. Measurement of diversity. Nature. 1949;163:688. https://doi.org/10.1038/163688a0.
Wang Y, Sheng H-F, He Y, Wu J-Y, Jiang Y-X, Tam NF-Y, et al. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl Environ Microbiol. 2012;78(23):8264–71. https://doi.org/10.1128/aem.01821-12.
Harrabi M, Alexandrino DAM, Aloulou F, Elleuch B, Liu B, Jia Z, et al. Biodegradation of oxytetracycline and enrofloxacin by autochthonous microbial communities from estuarine sediments. Sci Total Environ. 2019;648:962–72. https://doi.org/10.1016/j.scitotenv.2018.08.193.
Huang K, Tang J, Zhang X-X, Xu K, Ren H. A comprehensive insight into tetracycline resistant bacteria and antibiotic resistance genes in activated sludge using next-generation sequencing. Int J Mol Sci. 2014;15(6):10083–100.
Santos F, Mucha AP, Alexandrino DAM, Almeida CMR, Carvalho MF. Biodegradation of enrofloxacin by microbial consortia obtained from rhizosediments of two estuarine plants. J Environ Manag. 2019;231:1145–53. https://doi.org/10.1016/j.jenvman.2018.11.022.
Terzic S, Udikovic-Kolic N, Jurina T, Krizman-Matasic I, Senta I, Mihaljevic I, et al. Biotransformation of macrolide antibiotics using enriched activated sludge culture: kinetics, transformation routes and ecotoxicological evaluation. J Hazard Mater. 2018;349:143–52. https://doi.org/10.1016/j.jhazmat.2018.01.055.
Tappe W, Herbst M, Hofmann D, Koeppchen S, Kummer S, Thiele B, et al. Degradation of sulfadiazine by Microbacterium lacus strain SDZm4, isolated from lysimeters previously manured with slurry from sulfadiazine-medicated pigs. Appl Environ Microbiol. 2013;79(8):2572–7. https://doi.org/10.1128/aem.03636-12.
Li B, Zhang T. Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol. 2010;44(9):3468–73. https://doi.org/10.1021/es903490h.
Zhang Y, Hu S, Zhang H, Shen G, Yuan Z, Zhang W. Degradation kinetics and mechanism of sulfadiazine and sulfamethoxazole in an agricultural soil system with manure application. Sci Total Environ. 2017;607–608:1348–56. https://doi.org/10.1016/j.scitotenv.2017.07.083.
Zhao X, Li Y, Yang L, Wang X, Chen Z, Shen J. Screen and study of tetracycline-degrading bacteria from activated sludge and granular sludge. CLEAN—Soil, Air, Water. 2018;46(7):1700411. doihttps://doi.org/10.1002/clen.201700411.
Huang M, Tian S, Chen D, Zhang W, Wu J, Chen L. Removal of sulfamethazine antibiotics by aerobic sludge and an isolated Achromobacter sp. S-3. J Environ Sci. 2012;24(9):1594–9. https://doi.org/10.1016/S1001-0742(11)60973-X.
Reis PJ, Reis AC, Ricken B, Kolvenbach BA, Manaia CM, Corvini PF, et al. Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1. J Hazard Mater. 2014;280:741–9. https://doi.org/10.1016/j.jhazmat.2014.08.039.
Asano N, Takeuchi M, Ninomiya K, Kameda Y, Matsui K. Microbial degradation of Validamycin a by Flavobacterium Saccharophilum. J Antibiot. 1984;37(8):859–67.
Alexandrino DAM, Mucha AP, Almeida CMR, Gao W, Jia Z, Carvalho MF. Biodegradation of the veterinary antibiotics enrofloxacin and ceftiofur and associated microbial community dynamics. Sci Total Environ. 2017;581–582:359–68. https://doi.org/10.1016/j.scitotenv.2016.12.141.
Yang C-W, Tsai L-L, Chang B-V. Fungi extracellular enzyme-containing microcapsules enhance degradation of sulfonamide antibiotics in mangrove sediments. Environ Sci Pollut Res. 2018;25(10):10069–79. https://doi.org/10.1007/s11356-018-1332-8.
Zhang L, Yue Q, Yang K, Zhao P, Gao B. Analysis of extracellular polymeric substances (EPS) and ciprofloxacin-degrading microbial community in the combined Fe-C micro-electrolysis-UBAF process for the elimination of high-level ciprofloxacin. Chemosphere. 2018;193:645–54. https://doi.org/10.1016/j.chemosphere.2017.11.056.
Tahrani L, Mehri I, Reyns T, Anthonissen R, Verschaeve L, Khalifa ABH, et al. UPLC-MS/MS analysis of antibiotics in pharmaceutical effluent in Tunisia: ecotoxicological impact and multi-resistant bacteria dissemination. Arch Microbiol. 2018;200(4):553–65. https://doi.org/10.1007/s00203-017-1467-x.
Yan N, Xia S, Xu L, Zhu J, Zhang Y, Rittmann BE. Internal loop photobiodegradation reactor (ILPBR) for accelerated degradation of sulfamethoxazole (SMX). Appl Microbiol Biotechnol. 2012;94(2):527–35. https://doi.org/10.1007/s00253-011-3742-0.
Stolze Y, Eikmeyer F, Wibberg D, Brandis G, Karsten C, Krahn I, et al. IncP-1β plasmids of Comamonas sp. and Delftia sp. strains isolated from a wastewater treatment plant mediate resistance to and decolorization of the triphenylmethane dye crystal violet. Microbiology. 2012;158(8):2060–72. https://doi.org/10.1099/mic.0.059220-0.
Singhal L, Kaur P, Gautam V. Stenotrophomonas maltophilia: from trivial to grievous. Indian J Med Microbiol. 2017;35(4):469–79. https://doi.org/10.4103/ijmm.IJMM_16_430.
Leng Y, Bao J, Chang G, Zheng H, Li X, Du J, et al. Biotransformation of tetracycline by a novel bacterial strain Stenotrophomonas maltophilia DT1. J Hazard Mater. 2016;318:125–33. https://doi.org/10.1016/j.jhazmat.2016.06.053.
Pereira JHOS, Reis AC, Homem V, Silva JA, Alves A, Borges MT, et al. Solar photocatalytic oxidation of recalcitrant natural metabolic by-products of amoxicillin biodegradation. Water Res. 2014;65:307–20. https://doi.org/10.1016/j.watres.2014.07.037.
Meade MJ, Waddell RL, Callahan TM. Soil bacteria Pseudomonas putida and Alcaligenes xylosoxidans subsp. denitrificans inactivate triclosan in liquid and solid substrates. FEMS Microbiol Lett. 2001;204(1):45–8. https://doi.org/10.1111/j.1574-6968.2001.tb10860.x.
Larcher S, Yargeau V. Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biotechnol. 2011;91(1):211–8. https://doi.org/10.1007/s00253-011-3257-8.
Zhou N-Q, Liu D-F, Min D, Cheng L, Huang X-N, Tian L-J, et al. Continuous degradation of ciprofloxacin in a manganese redox cycling system driven by Pseudomonas putida MnB-1. Chemosphere. 2018;211:345–51. https://doi.org/10.1016/j.chemosphere.2018.07.117.
Sabic M, Cizmek L, Domanovac MV, Mestrovic E. Biodegradation of erythromycin with environmental microorganism Pseudomonas aeruginosa 3011. Chem Biochem Eng Q. 2015;29(3):367–73.
Jiang B, Li A, Cui D, Cai R, Ma F, Wang Y. Biodegradation and metabolic pathway of sulfamethoxazole by Pseudomonas psychrophila HA-4, a newly isolated cold-adapted sulfamethoxazole-degrading bacterium. Appl Microbiol Biotechnol. 2014;98(10):4671–81. https://doi.org/10.1007/s00253-013-5488-3.
Taweetanawanit P, Ratpukdi T, Siripattanakul-Ratpukdi S. Performance and kinetics of triclocarban removal by entrapped Pseudomonas fluorescens strain MC46. Bioresour Technol. 2019;274:113–9. https://doi.org/10.1016/j.biortech.2018.11.085.
Hwang W, Yoon SS. Virulence characteristics and an action mode of antibiotic resistance in multidrug-resistant Pseudomonas aeruginosa. Sci Rep. 2019;9(1):487. https://doi.org/10.1038/s41598-018-37422-9.
Funding
This study was partially funded by Office of Higher Education Commission (OHEC) and the S&T Postgraduate Education, Research Development Office (PERDO) for the support of their research program in Hazardous Substance Management in the Agricultural Industry through the Center of Excellence on Hazardous Substance Management. One researcher was partially financial support from Chulalongkorn Graduate School Thesis Grant. Some instrument used in this study was acquired through the King Mongkut’s University of Technology Thonburi 55th Anniversary Commemorative Fund.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 704 kb)
Rights and permissions
About this article
Cite this article
Nguyen, X.T.K., Pinyakong, O. & Thayanukul, P. Bacterial community structures and biodegradation kinetic of Tiamulin antibiotic degrading enriched consortia from swine wastewater. J Environ Health Sci Engineer 17, 1121–1130 (2019). https://doi.org/10.1007/s40201-019-00426-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40201-019-00426-2