Elsevier

Environmental Pollution

Volume 332, 1 September 2023, 121922
Environmental Pollution

Removal of tetracycline in nitrification membrane bioreactors with different ammonia loading rates: Performance, metabolic pathway, and key contributors

https://doi.org/10.1016/j.envpol.2023.121922Get rights and content

Highlights

  • Excellent nitrification performance and high TC removal efficiency were achieved.

  • Higher ALRs promoted the removal of TC at lower influent TC concentration.

  • Biodegradation was the major mechanism responsible for the removal of TC.

  • TC had no obvious effect on MBR performance.

Abstract

Membrane bioreactors (MBRs) have been widely applied for the treatment of wastewater that contains high concentrations of both ammonium and antibiotics. Nonetheless, information about tetracycline (TC) removal in nitrification MBRs with high ammonium loading rates (ALRs) is still very limited. Herein, the fate of TC at four different concentrations of 1, 5, 20, and 50 mg/L in three parallel lab-scale nitrification MBRs with different ALRs (named AN50, AN500, and AN1000) were investigated in this study. Excellent nitrification performance and high TC removal efficiency (90.46%) were achieved in AN1000 at influent TC concentration of 50 mg/L. Higher ALRs promoted the removal of TC at lower influent TC concentration (≤5 mg/L), while no significant difference was observed in TC removal efficiencies among different ALRs MBRs at higher influent TC concentration (≥20 mg/L), implying that the heterotrophic degradation could be strengthened after long-term exposure to high concentration of TC. Batch tests demonstrated that adsorption and biodegradation were the primary TC removal routes by nitrification sludge, of which both autotrophic ammonia oxidizers and heterotrophic microorganisms played an important role in the biodegradation of TC. FT-IR spectroscopy confirmed that amide groups on the sludge biomass contributed to the adsorption of TC. Mass balance analyses indicated that biodegradation (63.4–88.6% for AN50, 74.5–88.4% for AN500 and 74.4–91.4% for AN1000) was the major mechanism responsible for the removal of TC in nitrification MBRs, and its contribution increased with influent TC concentration, while only 1.1%–15.0% of TC removal was due to biosorption. TC was progressively degraded to small molecules and the presence of TC had no notable effect on membrane permeability. These jointly confirmed TC could be effectively removed via initial adsorption and subsequent biodegradation, while biodegradation was the primary mechanism in this study.

Introduction

Tetracyclines (TCs) are one of the most widely used broad-spectrum antibiotics in the livestock and aquaculture industries (Huang et al., 2020). A recent study showed that the average concentrations of TCs in soil and surface water in China were significantly higher than those of quinolones, macrolides, and sulfonamides (Lyu et al., 2020). A large amount of wastewater rich in NH4+-N and TC is generated in the pharmaceutical industry, and the traditional treatment methods have limited removal effect on TC (Zhang et al., 2006). In addition, animal farm wastewater was also characterized by high NH4+-N and TC concentrations (Zhou et al., 2013), which poses a significant risk of antibiotics resistance gene transmission (Chen et al., 2022). Therefore, it is of great importance to develop an efficient, stable, and economical process to control both NH4+-N and antibiotic pollution in response to the urgent need for ammonium-rich antibiotic wastewater treatment.

Biological treatment processes are expected to be an eco-friendly and cost-effective technique for handling antibiotic wastewater (Fischer & Majewsky, 2014), and it has been demonstrated that biodegradation and adsorption are two of the most important removal mechanisms of antibiotics during biological wastewater treatment processes (Yu et al., 2018). An extended sludge retention time (SRT) and a high sludge concentration is generally thought to be beneficial for the removal of both NH4+-N and antibiotics (Kumwimba & Meng, 2019). Membrane bioreactors (MBRs) can achieve complete sludge retention for attaining high sludge concentrations and long SRTs by effective biomass-effluent separation with membrane modules, providing sufficient time for the growth of slow-growing microorganisms like ammonia oxidizing bacteria (AOB) (Shen et al., 2014) and contributing to the development of specialized microbial species capable of decomposing compounds (such as antibiotics) of lower biodegradability (Shao et al., 2019; Shi et al., 2021). The combination of these factors suggests that MBRs may be more advantageous in terms of high NH4+-N antibiotic wastewater treatment.

In addition, a large number of studies have been reported that AOB were capable of improving the degradation of a wide range of toxic or refractory organic pollutants (Joss et al., 2006; Park et al., 2017). For example, Park et al. (2017) performed batch tests using activated sludge from a MBR and demonstrated AOB make a huge contribution to the removal of a variety of micropollutants. Much evidence confirmed the contributions of AOB to the biodegradation of TC, and suggested that ammonia monooxygenase (AMO), a key enzyme of AOB catalyzing the first step of ammonia oxidation to nitrite, played a pivotal role in the co-metabolism of TC (Shi et al., 2011; Wang et al., 2021; Yang et al., 2023). In our previous studies, we found that the abundance of AOB and the ammonia oxidation activity of sludge in MBR increased with the elevation of NH4+-N loading rates (ALRs) within a certain range (Wang et al., 2016; Xu et al., 2022). Thus, the highly activated nitrifying sludge in MBR with high ALRs is expected to play a more significant role in enhancing TC removal. Although MBRs have been widely adopted to treat antibiotic pharmaceutical wastewater (Hou et al., 2016; Xiao et al., 2019), and been confirmed to be able to efficiently remove NH4+-N and TC simultaneously (Sheng et al., 2018), the influent NH4+-N concentration in most studies was generally lower than that of 300 mg/L (Sheng et al., 2018), information about TC removal in MBRs with high ALRs is still very limited. Meanwhile, the presence of high TC concentrations in wastewater may affect the nitrification process. Katipoglu-Yazan et al. (2015) found that 50 mg/L of TC caused the nitrifying bacteria to be phased out, eventually leading to complete inhibition of the nitrification capacity of the sludge. Thus, the effects of high concentrations of TC on the performance of MBR with high ALRs should also be studied.

In this study, three parallel lab-scale nitrification MBRs with different ALRs were operated (named AN50, AN500, and AN1000) with the increasing TC dosage (1 mg/L-50 mg/L). The TC removal efficiencies, removal routes and metabolic pathway in MBRs were determined. The influences of TC, in turn, on the nitrification performances of MBRs were also evaluated. This study demonstrated the potential of MBR in the treatment of wastewater with high concentrations of TC and ammonia nitrogen.

Section snippets

Experiment setup and operating conditions

Three sets of lab-scale MBRs were operated, all with an effective volume of 2 L and a hydraulic retention time of 14 h. The membrane modules were made of PVDF hollow fiber membrane with a pore size of 0.05 μm and a membrane flux of 7.5 L/(m2·h). The influent and effluent of the MBRs were realized by peristaltic pumps. Pressure sensors were installed between the membrane modules and effluent pumps to record the variation in transmembrane pressure. Aeration was performed with blower pumps

Tetracycline removal

The other operating conditions of the three MBRs with different NH4+-N loads were maintained constant, and the TC concentration in the influent was gradually increased in stages, in the order of 1, 5, 20, and 50 mg/L. The TC concentration in the effluent during operation is recorded in Fig. 1(A), and the removal rate statistics are shown in Fig. 1(B). At an influent TC concentration of 1 mg/L, the removal rate of AN50 was close to 90% in the first week and then decreased to about 80%, which may

Conclusions

The removal efficiency of TC by MBRs with different ALRs and the interaction between TC and nitrification sludge were investigated. The results confirmed that three MBRs with different ALRs (AN50, AN500, and AN1000) could achieve efficient simultaneous removal of ammonia and TC when the influent TC concentration increased in a gradient of 1, 5, 20, 50 mg/L. AN500 and AN1000 exhibited higher removal rates than AN50 at low concentrations (≤5 mg/L). In contrast, when raised to 20 and even 50 mg/L,

Credit authors statement

Huaihao Xu: Methodology, Data curation, analysis, preparing original draft; Yuepeng Deng: Methodology, analysis; Mingji Li: Analysis; Kaoming Zhang: Analysis, Data curation; Jie Zou: Data curation; Yunhua Yang: Reviewing and editing; Peng Shi: Reviewing and editing; Yiping Feng: Reviewing and editing; Chun Hu: Resources, reviewing and editing; Zhu Wang: Resources, analysis, Methodology, reviewing and editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We gratefully acknowledge the generous support provided by NSFC (51608134 and 52070047), Guangzhou city science and technology project (202102010460 and 2023A03J0082), Guangdong natural science foundation (2021A1515011898 and 2023A1515012324), Featured Innovation Project of Guangdong Education Department (2019KTSCX135), State Key Laboratory of Pollution Control and Resource Reuse Foundation (PCRRF19010) and Innovation and Entrepreneurship Training Program for College Students (202211078141).

References (51)

  • H. Liu et al.

    Fate of tetracycline in enhanced biological nutrient removal process

    Chemosphere

    (2018)
  • J. Lyu et al.

    Antibiotics in soil and water in China-a systematic review and source analysis

    Environ. Pollut.

    (2020)
  • T.T. More et al.

    Extracellular polymeric substances of bacteria and their potential environmental applications

    J. Environ. Manag.

    (2014)
  • J. Park et al.

    Removal of pharmaceuticals and personal care products by ammonia oxidizing bacteria acclimated in a membrane bioreactor: contributions of cometabolism and endogenous respiration

    Sci. Total Environ.

    (2017)
  • L.W. Shen et al.

    Reactor performance and microbial ecology of a nitritation membrane bioreactor

    J. Membr. Sci.

    (2014)
  • B. Sheng et al.

    Interactive effects between tetracycline and nitrosifying sludge microbiota in a nitritation membrane bioreactor

    Chem. Eng. J.

    (2018)
  • Y.H. Shi et al.

    Exploiting extracellular polymeric substances (EPS) controlling strategies for performance enhancement of biological wastewater treatments: an overview

    Chemosphere

    (2017)
  • Y.J. Shi et al.

    Sorption and biodegradation of tetracycline by nitrifying granules and the toxicity of tetracycline on granules

    J. Hazard Mater.

    (2011)
  • Z. Tan et al.

    The survival and removal mechanism of Sphingobacterium changzhouense TC931 under tetracycline stress and its' ecological safety after application

    Bioresour. Technol.

    (2021)
  • J.B. Wang et al.

    Evaluating tetracycline degradation pathway and intermediate toxicity during the electrochemical oxidation over a Ti/Ti4O7 anode

    Water Res.

    (2018)
  • X.C. Wang et al.

    The performance of aerobic granular sludge for simulated swine wastewater treatment and the removal mechanism of tetracycline

    J. Hazard Mater.

    (2021)
  • Z. Wang et al.

    Response of performance and ammonia oxidizing bacteria community to high salinity stress in membrane bioreactor with elevated ammonia loading

    Bioresour. Technol.

    (2016)
  • J. Wu et al.

    Application of response surface methodology to the removal of the antibiotic tetracycline by electrochemical process using carbon-felt cathode and DSA (Ti/RuO2-IrO2) anode

    Chemosphere

    (2012)
  • K. Xiao et al.

    Current state and challenges of full-scale membrane bioreactor applications: a critical review

    Bioresour. Technol.

    (2019)
  • Z. Xie et al.

    Construction of carbon dots modified MoO3/g-C3N4 Z-scheme photocatalyst with enhanced visible-light photocatalytic activity for the degradation of tetracycline

    Appl. Catal. B Environ.

    (2018)
  • Cited by (4)

    This paper has been recommended for acceptance by Yaoyu Zhou.

    View full text