Skip to main content
SpringerLink
Log in

Different inhibitory mechanisms of chlortetracycline and enrofloxacin on mesophilic anaerobic degradation of propionate

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

Abstract

In anaerobic digestion, propionate is a key intermediate whose degradation is thermodynamically challenging and accumulation is detrimental to the process. Many wastewater streams contain antibiotics due to its globally increasing use, and these compounds can inhibit methane production. However, the effect of antibiotics on propionate degradation in anaerobic digestion remains unclear. In this study, the influence of two antibiotics (chlortetracycline [CTC] and enrofloxacin [EFX]) on biogas production and mesophilic propionate-degrading microbial community was investigated. CTC strongly repressed propionate oxidation, acetate utilization, and methane production, while EFX only inhibited propionate oxidation and methane production to a lesser extent. Microbial community analyses showed that syntrophic propionate-oxidizing bacteria (SPOB) Syntrophobacter had strong tolerance to both CTC and EFX. CTC inhibition mainly acted on the activity of acetate-oxidizing bacteria (Mesotoga, Geovibrio, Tepidanaerobacter, unclassified Bacteroidetes, and unclassified Clostridia) and acetoclastic methanogen, while EFX inhibition applied to the SPOB Smithella and acetoclastic methanogen. Network analysis further indicated that more complicated correlation among bacterial genera occurred in CTC treatments. These results suggested that CTC and EFX inhibited propionate degradation via different mechanisms, which was the result of joint action by antibiotics and microbial interactions.

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

  • Akyol Ç, Aydin S, Ince O, Ince B (2016) A comprehensive microbial insight into single-stage and two-stage anaerobic digestion of oxytetracycline-medicated cattle manure. Chem Eng J 303:675–684

    CAS  Google Scholar 

  • Álvarez JA, Otero L, Lema JM, Omil F (2010) The effect and fate of antibiotics during the anaerobic digestion of pig manure. Bioresour Technol 101:8581–8586

    Google Scholar 

  • Aydin S, Cetecioglu Z, Arikan O, Ince B, Ozbayram EG, Ince O (2015a) Inhibitory effects of antibiotic combinations on syntrophic bacteria, homoacetogens and methanogens. Chemosphere 120:515–520

    CAS  Google Scholar 

  • Aydin S, Ince B, Ince O (2015b) Application of real-time PCR to determination of combined effect of antibiotics on Bacteria, methanogenic Archaea, Archaea in anaerobic sequencing batch reactors. Water Res 76:88–98

    CAS  Google Scholar 

  • Bae HS, Im WT, Suwa Y, Lee JM, Lee ST, Chang YK (2009) Characterization of diverse heterocyclic amine-degrading denitrifying bacteria from various environments. Arch Microbiol 191:329–340

    CAS  Google Scholar 

  • Bauer A, Lizasoain J, Nettmann E et al (2014) Effects of the antibiotics chlortetracycline and enrofloxacin on the anaerobic digestion in continuous experiments. Bioenerg Res 7:1244–1252

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Caccavo FJ, Coates JD, Rossello-Mora RA, Ludwig W, Schleifer KH, Lovley DR, Mcinerney MJ (1996) Geovibrio ferrireducens, a phylogenetically distinct dissimilatory Fe(III)-reducing bacterium. Arch Microbiol 165:370–376

    CAS  Google Scholar 

  • Cetecioglu Z, Ince B, Orhon D, Ince O (2012) Acute inhibitory impact of antimicrobials on acetoclastic methanogenic activity. Bioresour Technol 114:109–116

    CAS  Google Scholar 

  • Cetecioglu Z, Ince B, Gros M, Rodriguez-Mozaz S, Barceló D, Orhon D, Ince O (2013) Chronic impact of tetracycline on the biodegradation of an organic substrate mixture under anaerobic conditions. Water Res 47:2959–2969

    CAS  Google Scholar 

  • Cetecioglu Z, Ince B, Orhon D, Ince O (2016) Anaerobic sulfamethoxazole degradation is driven by homoacetogenesis coupled with hydrogenotrophic methanogenesis. Water Res 90:79–89

    CAS  Google Scholar 

  • Chen JL, Ortiz R, Steele TWJ, Stuckey DC (2014) Toxicants inhibiting anaerobic digestion: a review. Biotechnol Adv 32:1523–1534

    Google Scholar 

  • Cheng DL, Ngo HH, Guo WS et al (2018) Problematic effects of antibiotics on anaerobic treatment processes in swine wastewater. Bioresour Technol 263:642–653

    CAS  Google Scholar 

  • Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260

    CAS  Google Scholar 

  • de Bok FAM, Stams AJM, Dijkema C, Boone DR (2001) Pathway of Propionate Oxidation by a Syntrophic Culture of Smithella propionica and Methanospirillum hungatei. Applied and Environmental Microbiology 67 (4):1800–1804

    CAS  Google Scholar 

  • 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 7:173–190

    CAS  Google Scholar 

  • Deng YQ, Zhang Y, Gao YX, Li D, Liu R, Liu M, Zhang H, Hu B, Yu T, Yang M (2012) Microbial community compositional analysis for series reactors treating high level antibiotic wastewater. Environ Sci Technol 46:795–801

    CAS  Google Scholar 

  • Griffiths RI, Whiteley AS (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491

    CAS  Google Scholar 

  • Hou J, Wan WN, Mao DQ, Wang C, Mu QH, Qin SY, Luo Y (2015) Occurrence and distribution of sulfonamides, tetracyclines, quinolones, macrolides, and nitrofurans in livestock manure and amended soils of Northern China. Environ Sci Pollut R 22:4545–4554

    CAS  Google Scholar 

  • Houwen FP, Plokker J, Stams AJM, Zehnder AJB (1990) Enzymatic evidence for involvement of the methylmalonyl-CoA pathway in propionate oxidation by Syntrophobacter wolinii. Archives of Microbiology 155 (1):52–55

    CAS  Google Scholar 

  • Huang MH, Qi FF, Wang J, Xu Q, Lin L (2015) Changes of bacterial diversity and tetracycline resistance in sludge from AAO systems upon exposure to tetracycline pressure. J Hazard Mater 298:303–309

    CAS  Google Scholar 

  • Ito T, Yoshiguchi K, Ariesyady HD, Okabe S (2011) Identification of a novel acetate-utilizing bacterium belonging to Synergistes group 4 in anaerobic digester sludge. ISME J 5:1844–1856

    CAS  Google Scholar 

  • Ji JY, Xing YJ, Ma ZT, Zhang M, Zheng P (2013) Acute toxicity of pharmaceutical wastewaters containing antibiotics to anaerobic digestion treatment. Chemosphere 91 (8):1094–1098

    CAS  Google Scholar 

  • Jiang X, Hayashi J, Sun ZY et al (2013) Improving biogas production from protein-rich distillery wastewater by decreasing ammonia inhibition. Process Biochem 48:1778–1784

    CAS  Google Scholar 

  • Li JZ, Ban QY, Zhang LG, Jha AK (2012) Syntrophic propionate degradation in anaerobic digestion: a review. Int J Agric Biol 14:843–850

    CAS  Google Scholar 

  • Lu Y, Liaquat R, Astals S, Jensen PD, Batstone DJ, Tait S (2018) Relationship between microbial community, operational factors and ammonia inhibition resilience in anaerobic digesters at low and moderate ammonia background concentrations. New Biotechnol 44:23–30

    CAS  Google Scholar 

  • Marzo A, Bo LD (1998) Chromatography as an analytical tool for selected antibiotic classes: a reappraisal addressed to pharmacokinetic applications. J Chromatogr A 812:17–34

    CAS  Google Scholar 

  • Nobu MK, Narihiro T, Rinke C, Kamagata Y, Tringe SG, Woyke T, Liu WT (2015) Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J 9:1710–1722

    Google Scholar 

  • Ozbayram EG, Arikan O, Ince B, Cetecioglu Z, Aydin S, Ince O (2015) Acute effects of various antibiotic combinations on acetoclastic methanogenic activity. Environ Sci Pollut R 22:6230–6235

    CAS  Google Scholar 

  • Pulicharla R, Das RK, Brar SK, Drogui P, Sarma SJ, Verma M, Surampalli RY, Valero JR (2015) Toxicity of chlortetracycline and its metal complexes to model microorganisms in wastewater sludge. Sci Total Environ 532:669–675

    CAS  Google Scholar 

  • Quan ZX, Im WT, Lee ST (2006) Azonexus caeni sp. nov., a denitrifying bacterium isolated from sludge of a wastewater treatment plant. Int J Syst Evol Microbiol 56:1043–1046

    CAS  Google Scholar 

  • Rajagopal R, Massé DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour Technol 143:632–641

    CAS  Google Scholar 

  • Sanz JL, Rodríguez N, Amils R (1996) The action of antibiotics on the anaerobic digestion process. Applied Microbiology and Biotechnology 46 (5-6):587–592

    CAS  Google Scholar 

  • Shigematsu T, Tang YQ, Kawaguchi H, Ninomiya K, Kijima J, Kobayashi T, Morimura S, Kida K (2003) Effect of dilution rate on structure of a mesophilic acetate-degrading methanogenic community during continuous cultivation. J Biosci Bioeng 96:547–558

    CAS  Google Scholar 

  • Shigematsu T, Era S, Mizuno Y, Ninomiya K, Kamegawa Y, Morimura S, Kida K (2006) Microbial community of a mesophilic propionate-degrading methanogenic consortium in chemostat cultivation analyzed based on 16S rRNA and acetate kinase genes. Appl Microbiol Biotechnol 72:401–415

    CAS  Google Scholar 

  • 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 43:4740–4750

    CAS  Google Scholar 

  • Takuya H, Takashi F, Akio T (2013) Aminivibrio pyruvatiphilus gen. nov., sp. nov., an anaerobic, amino-acid-degrading bacterium from soil of a Japanese rice field. Int J Syst Evol Microbiol 63:3679–3686

    Google Scholar 

  • Tao CW, Hsu BM, Ji WT, Hsu TK, Kao PM, Hsu CP, Shen SM, Shen TY, Wan TJ, Huang YL (2014) Evaluation of five antibiotic resistance genes in wastewater treatment systems of swine farms by real-time PCR. Sci Total Environ 496:116–121

    CAS  Google Scholar 

  • Wang HZ, Gou M, Yi Y, Xia ZY, Tang YQ (2018a) Identification of novel potential acetate-oxidizing bacteria in an acetate-fed methanogenic chemostat based on DNA stable isotope probing. J Gen Appl Microbiol 64:221–231

    CAS  Google Scholar 

  • Wang R, Zhang J, Liu J et al (2018b) Effects of chlortetracycline, Cu and their combination on the performance and microbial community dynamics in swine manure anaerobic digestion. J Environ Sci 67:209–218

    Google Scholar 

  • Werner JJ, Garcia ML, Perkins SD, Yarasheski KE, Smith SR, Muegge BD, Stadermann FJ, DeRito C, Floss C, Madsen EL, Gordon JI, Angenent LT (2014) Microbial community dynamics and stability during an ammonia-induced shift to syntrophic acetate oxidation. Appl Environ Microbiol 80:3375–3383

    Google Scholar 

  • Westerholm M, Roos S, Schnürer A (2011) Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes. Syst Appl Microbiol 34:260–266

    CAS  Google Scholar 

  • Xie WY, Shen Q, Zhao FJ (2017) Antibiotics and antibiotic resistance from animal manures to soil: a review: antibiotics and antibiotic resistance. Eur J Soil Sci 69:181–195

    Google Scholar 

  • Xiong YH, Harb M, Hong PY (2017) Performance and microbial community variations of anaerobic digesters under increasing tetracycline concentrations. Appl Microbiol Biotechnol 101:5505–5517

    CAS  Google Scholar 

  • Yang ZM, Xu XH, Guo RB, Fan XL, Zhao XX (2015) Accelerated methanogenesis from effluents of hydrogen-producing stage in anaerobic digestion by mixed cultures enriched with acetate and nano-sized magnetite particles. Bioresour Technol 190:132–139

    CAS  Google Scholar 

  • Yang G, Zhang GM, Zhuan R, Yang A, Wang Y (2016a) Transformations, inhibition, and inhibition control methods of sulfur in sludge anaerobic digestion: a review. Curr Org Chem 20:2780–2789

    CAS  Google Scholar 

  • Yang ZM, Guo RB, Shi XS, Wang CS, Lin W, Meng D (2016b) Magnetite nanoparticles enable a rapid conversion of volatile fatty acids to methane. RSC Adv 6:25662–25668

    CAS  Google Scholar 

  • Yin FB, Dong HM, Ji C, Tao XP, Chen YX (2016) Effects of anaerobic digestion on chlortetracycline and oxytetracycline degradation efficiency for swine manure. Waste Manag 56:540–546

    CAS  Google Scholar 

  • Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015) Comprehensive evaluation of antibiotics emission and fate in the river basins of china: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Technol 49:6772–6782

    CAS  Google Scholar 

  • Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075

    CAS  Google Scholar 

Download references

Funding

This work was supported by the Ministry of Science and Technology of China (No. 2016YFE0127700) and the National Natural Science Foundation of China (No. 51678378 and No. 51808361).

Author information

Authors and Affiliations

  1. College of Architecture and Environment, Sichuan University, No. 24, South Section 1, First Ring Road, Chengdu, 610065, Sichuan, China

    Min Gou, HuiZhong Wang, Jie Li, ZhaoYong Sun & YueQin Tang

  2. College of Engineering, Peking University, No. 5 Yiheyuan Road, Haidian District, Beijing, 100871, China

    Yong Nie

  3. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Central 6, Higashi 1-1-1, Tsukuba, Ibaraki, 305-8566, Japan

    Masaru Konishi Nobu

Authors
  1. Min Gou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. HuiZhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. ZhaoYong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yong Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Masaru Konishi Nobu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. YueQin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to YueQin Tang.

Additional information

Responsible Editor: Gerald Thouand

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 306 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gou, M., Wang, H., Li, J. et al. Different inhibitory mechanisms of chlortetracycline and enrofloxacin on mesophilic anaerobic degradation of propionate. Environ Sci Pollut Res 27, 1406–1416 (2020). https://doi.org/10.1007/s11356-019-06705-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06705-7

Keywords

Search

Navigation