Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2021, Vol. 15 Issue (1) : 17    https://doi.org/10.1007/s11783-020-1309-y
REVIEW ARTICLE
A review on anammox process for the treatment of antibiotic-containing wastewater: Linking effects with corresponding mechanisms
Jinjin Fu, Quan Zhang, Baocheng Huang, Niansi Fan(), Rencun Jin()
Laboratory of Water Pollution Remediation, School of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, China
 Download: PDF(753 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

• Anammox is promising for nitrogen removal from antibiotic-containing wastewater.

• Most antibiotics could inhibit the anammox performance and activity.

• Antibiotic pressure promoted the increase in antibiotic resistance genes (ARGs).

• Antibiotic-resistance mechanisms of anammox bacteria are speculated.

Antibiotic is widely present in the effluent from livestock husbandry and the pharmaceutical industry. Antibiotics in wastewater usually have high biological toxicity and even promote the occurrence and transmission of antibiotic resistant bacteria and antibiotic resistance genes. Moreover, most antibiotic-containing wastewater contains high concentration of ammonia nitrogen. Improper treatment will lead to high risk to the surrounding environment and even human health. The anaerobic ammonium oxidation (anammox) with great economic benefit and good treatment effect is a promising process to remove nitrogen from antibiotic-containing wastewater. However, antibiotic inhibition has been observed in anammox applications. Therefore, a comprehensive overview of the single and combined effects of various antibiotics on the anammox system is conducted in this review with a focus on nitrogen removal performance, sludge properties, microbial community, antibiotic resistance genes and anammox-involved functional genes. Additionally, the influencing mechanism of antibiotics on anammox consortia is summarized. Remaining problems and future research needs are also proposed based on the presented summary. This review provides a better understanding of the influences of antibiotics on anammox and offers a direction to remove nitrogen from antibiotic-containing wastewater by the anammox process.

Keywords Anammox      Antibiotic      Mechanism      Inhibition     
Corresponding Author(s): Niansi Fan,Rencun Jin   
Issue Date: 26 August 2020
 Cite this article:   
Jinjin Fu,Quan Zhang,Baocheng Huang, et al. A review on anammox process for the treatment of antibiotic-containing wastewater: Linking effects with corresponding mechanisms[J]. Front. Environ. Sci. Eng., 2021, 15(1): 17.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-020-1309-y
https://academic.hep.com.cn/fese/EN/Y2021/V15/I1/17
Reactor Antibiotic Antibiotic concentration Operating days NLR (kg N/(m3·d)) NRR (kg N/(m3·d)) Reference
Before adding After adding Before adding After adding
UASB Oxytetracycline 0.1–1 mg/L 156 20.0 14.3±2.9 Zhang et al. (2019a)
Sulfamethoxazole 13.2±2.7
Oxytetracycline and Sulfamethoxazole 15.2±1.9
UASB Oxytetracycline 1 and 2 mg/L 42 5.50 1.20±0.09 Shi et al. (2017)
UAF Erythromycin 0.01–50 mg/L 120 0.34 0.17 Zhang et al. (2019b)
Biofilm reactor Tetracycline 10 mg/L
100 mg/L
1000 mg/L
200–306
307–418
419–518
0.89±0.06 0.56±0.05 0.56±0.04
0.64±0.04
0.49±0.04
Meng et al. (2019)
FBAS Chlortetracycline 60 mg/L
20 mg/L
71–84
85–94
0.75±0.05
0.85±0.02
0.85±0.02
0.32±0.00
0.57±0.12
0.48±0.10
0.48±0.10
0.11±0.02
Yao et al. (2018)
UASB Oxytetracycline 50 mg/L 26 12.4 2 Yang et al. (2013)
UASB Oxytetracycline 6, 12.5, 25, 50 mg/L 57 12.4±1.3 5.0±5.5 Zhang et al. (2013)
Cylindrical Biofilter Norfloxacin 0.001, 1, 10, 50, 100 mg/L 150 0.345 0.198 Zhang et al. (2018c)
UASB Tetracycline 0.1, 0.2, 0.3, 0.5, 1.0 mg/L 110 7.25±0.22 7.20±0.16 3.2 Fan et al. (2019)
Tab.1  The effects of antibiotics on the performance of the anammox process.
Reactor Antibiotic Antibiotic concentration SAA Operating days Reference
SBR Chloramphenicol 6 mg/L 0.528–0.096 mg N/(mg VSS·d) 41 Phanwilai et al. (2020)
SBR Chloramphenicol
Tetracycline hydrochloride
20 mg/L
50 mg/L
0.25–0.05 g N/(g VSS·d) 20 Fernández et al. (2009)
Cylindrical Biofilter Norfloxacin
Erythromycin
1 mg/L 10.8–7.56 mg/(g SS·h)
10.83–10.65 mg/(g SS·h)
30 Zhang et al. (2019c)
UASB Amoxicillin
Florfenicol
Sulfamethazine
10, 30, 60, 80, 150 mg/L
10, 20, 15, 10, 5 mg/L
5, 20, 30, 80, 100, 200 mg/L
427.7 to ~500 mg TN/(g VSS·d)
430.4 to ~450 mg TN/(g VSS·d)
502.9 to ~450 mg TN/(g VSS·d)
80 Zhang et al. (2015)
UASB Oxytetracycline 6, 12.5, 25, 50 mg/L 16.6– 6.4±6.6 mg TN/(g VSS·h) 57 Zhang et al. (2013)
Cylindrical Biofilter Norfloxacin 0.001, 1, 10, 50, 100 mg/L 10.84 –7.56 mg/(g SS·h) 150 Zhang et al. (2018c)
UASB Spiramycin 0.5 mg/L 92.7±7.7–85.1 mg N/(g VSS·d) 65 Wu et al. (2020)
5 mg/L 92.7±7.7 to 47.19±14.1 mg N/(g VSS·d)
UASB Oxytetracycline 1 and 2 mg/L 347.7±5.3–58.76 mg N/(g VSS·d) 42 Shi et al. (2017)
Tab.2  Summary of the specific anammox activity in the presence of antibiotics
Antibiotic Antibiotic concentration Microbial species Varieties of relative abundance Reference
Oxytetracycline 0.1–1 mg/L Planctomycetes and Proteobacteria Decreased 26.2% Zhang et al. (2019a)
Sulfamethoxazole Decreased 15.9%
Tetracycline 100 mg/L Planctomycetes Increased 7.11% Meng et al. (2019)
Proteobacteria Increased 2.20%
1000 mg/L Planctomycetes Decreased 10.12%
Proteobacteria Decreased 16.91%
Norfloxacin 1 mg/L Planctomycetes Decreased 2.44% Zhang et al. (2019c)
Arenimonas 0
Erythromycin Planctomycetes Decreased 0.01%
Arenimonas Increased 4.54%
Sulfadimethoxine 5–7 mg/L Candidatus Brocadia Decreased 2.18% Du et al. (2018)
Norfloxacin 0.001, 1, 10, 50, 100 mg/L Candidatus Kuenenia Increased 4.54% Zhang et al. (2018c)
Tetracycline 0.1–1.5 mg/L Planctomycetes, Proteobacteria and Chloroflexi Decreased 10% Fan et al. (2019)
Erythromycin 0.01–100 mg/L Proteobacteria Increased 43.22% Zhang et al. (2019b)
Planctomycetes Decreased 21.91%
Tab.3  The dynamic variations of different AnAOB in anammox systems under antibiotics pressure.
Fig.1  Possible tolerance mechanism of AnAOB to OTC and SMX, adapted from (Zhang et al., 2019b) with permission.
Fig.2  Co-selection mechanism of antibiotic and metal resistant: (a) co-resistance mechanism; (b) cross-resistance mechanism; (c) co-regulation mechanism. Circles, triangles, and rectangles represent antibiotics, heavy metals and efflux pumps, respectively. Different colors show different substances mentioned above.
Anammox
ARGs
Anaerobic ammonium oxidation
Antibiotic resistance genes
MRGs Metal resistance genes
NRR Nitrogen removal rate
TC Tetracycline
OTC Oxytetracycline
CTC Chlortetracycline
PAR Acetaminophen
DOX Doxycycline
SDM Sulfadimethoxine
SM Sulfamethazine
CAP Chloramphenicol
SAA Specific anammox activity
SBR Sequential batch reactor
FBAS Integrated fixed-biofilm and activated sludge
CSTR Continuous stirred tank reactor
FF Florfenicol
AMX Amoxicillin
CIP Ciprofloxacin
NOR Norfloxacin
ERY Erythromycin
UAF Up-flow anaerobic biological filter
TNRE Total nitrogen removal efficiency
EPS Extracellular polymeric substances
PN Protein
PS Polysaccharide
SMX Sulfamethoxazole
HZO Hydrazine-oxidizing enzyme
HAO Hydroxylamine oxidoreductase
TCH Tetracycline hydrochloride
ARB Antibiotic resistant bacteria
AOB Ammonium oxidizing bacteria
QS Quorum sensing
BA Bio-augmentation
BAD Bio-augmentation dosage
BAT
TMP
Bio-augmentation time
Trimethoprim
  
1 M Ali, S Okabe (2015). Anammox-based technologies for nitrogen removal: Advances in process start-up and remaining issues. Chemosphere, 141: 144–153
https://doi.org/10.1016/j.chemosphere.2015.06.094
2 A Alighardashi, D Pandolfi, O Potier, M N Pons (2009). Acute sensitivity of activated sludge bacteria to erythromycin. Journal of Hazardous Materials, 172(2–3): 685–692
https://doi.org/10.1016/j.jhazmat.2009.07.051
3 T Alvarino, E Katsou, S Malamis, S Suarez, F Omil, F Fatone (2014). Inhibition of biomass activity in the via nitrite nitrogen removal processes by veterinary pharmaceuticals. Bioresource Technology, 152: 477–483
https://doi.org/10.1016/j.biortech.2013.10.107
4 T Alvarino, S Suarez, E Katsou, J Vazquez-Padin, J M Lema, F Omil (2015). Removal of PPCPs from the sludge supernatant in a one stage nitritation/anammox process. Water Research, 68: 701–709
https://doi.org/10.1016/j.watres.2014.10.055
5 C L Amorim, A S Maia, R B Mesquita, A O Rangel, M C Van Loosdrecht, M E Tiritan, P M Castro (2014). Performance of aerobic granular sludge in a sequencing batch bioreactor exposed to ofloxacin, norfloxacin and ciprofloxacin. Water Research, 50: 101–113
https://doi.org/10.1016/j.watres.2013.10.043
6 S Aydin, B Ince, O Ince (2016). Assessment of anaerobic bacterial diversity and its effects on anaerobic system stability and the occurrence of antibiotic resistance genes. Bioresource Technology, 207: 332–338
https://doi.org/10.1016/j.biortech.2016.01.080
7 C Baker-Austin, M S Wright, R Stepanauskas, J V Mcarthur (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4): 176–182
https://doi.org/10.1016/j.tim.2006.02.006
8 W Baran, E Adamek, J Ziemianska, A Sobczak (2011). Effects of the presence of sulfonamides in the environment and their influence on human health. Journal of Hazardous Materials, 196: 1–15
https://doi.org/10.1016/j.jhazmat.2011.08.082
9 W Ben, Z Qiang, X Pan, M Chen (2009). Removal of veterinary antibiotics from sequencing batch reactor (SBR) pretreated swine wastewater by Fenton’s reagent. Water Research, 43(17): 4392–4402
https://doi.org/10.1016/j.watres.2009.06.057
10 K D Brown, J Kulis, B Thomson, T H Chapman, D B Mawhinney (2006). Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico. Science of the Total Environment, 366(2–3): 772–783
https://doi.org/10.1016/j.scitotenv.2005.10.007
11 T T Chen, P Zheng, L D Shen (2013). Growth and metabolism characteristics of anaerobic ammonium-oxidizing bacteria aggregates. Applied Microbiology and Biotechnology, 97(12): 5575–5583
https://doi.org/10.1007/s00253-012-4346-z
12 Y F Cheng, G F Li, W J Ma, Y Xue, Q Liu, Z Z Zhang, R C Jin (2020). Resistance of anammox granular sludge to copper nanoparticles and oxytetracycline and restoration of performance. Bioresource Technology, 307: 123264
https://doi.org/10.1016/j.biortech.2020.123264
13 K I Cogert, R M Ziels, M K H Winkler (2019). Reducing cost and environmental impact of wastewater treatment with denitrifying methanotrophs, anammox, and mainstream anaerobic treatment. Environmental Science & Technology, 53(21): 12935–12944
https://doi.org/10.1021/acs.est.9b04764
14 N Collado, G Buttiglieri, E Marti, L Ferrando-Climent, S Rodriguez-Mozaz, D Barcelo, J Comas, I Rodriguez-Roda (2013). Effects on activated sludge bacterial community exposed to sulfamethoxazole. Chemosphere, 93(1): 99–106
https://doi.org/10.1016/j.chemosphere.2013.04.094
15 R Dafouz, N Cáceres, J L Rodríguez-Gil, N Mastroianni, M López de Alda, D Barceló, Á G de Miguel, Y Valcárcel. (2018). Does the presence of caffeine in the marine environment represent an environmental risk? A regional and global study. Science of the Total Environment, 615: 632–642
https://doi.org/10.1016/j.scitotenv.2017.09.155
16 A Dapena-Mora, I Fernández, J L Campos, A Mosquera-Corral, R Méndez, M S M Jetten (2007). Evaluation of activity and inhibition effects on Anammox process by batch tests based on the nitrogen gas production. Enzyme and Microbial Technology, 40(4): 859–865
https://doi.org/10.1016/j.enzmictec.2006.06.018
17 M de Cazes, R Abejon, M P Belleville, J Sanchez-Marcano (2014). Membrane bioprocesses for pharmaceutical micropollutant removal from waters. Membranes (Basel), 4(4): 692–729
https://doi.org/10.3390/membranes4040692
18 M S de Graaff, N M Vieno, K Kujawa-Roeleveld, G Zeeman, H Temmink, C J Buisman (2011). Fate of hormones and pharmaceuticals during combined anaerobic treatment and nitrogen removal by partial nitritation-anammox in vacuum collected black water. Water Research, 45(1): 375–383
https://doi.org/10.1016/j.watres.2010.08.023
19 J de Vrieze, S Gildemyn, R Vilchez-Vargas, R Jauregui, D H Pieper, W Verstraete, N Boon (2015). Inoculum selection is crucial to ensure operational stability in anaerobic digestion. Applied Microbiology and Biotechnology, 99(1): 189–199
https://doi.org/10.1007/s00253-014-6046-3
20 Y Deng, Y Zhang, Y Gao, D Li, R Liu, M Liu, H Zhang, B Hu, T Yu, M Yang (2012). Microbial community compositional analysis for series reactors treating high level antibiotic wastewater. Environmental Science & Technology, 46(2): 795–801
https://doi.org/10.1021/es2025998
21 J Ding, X L An, S B Lassen, H T Wang, D Zhu, X Ke (2019). Heavy metal-induced co-selection of antibiotic resistance genes in the gut microbiota of collembolans. Science of the Total Environment, 683: 210–215
https://doi.org/10.1016/j.scitotenv.2019.05.302
22 S Ding, J Wu, M Zhang, H Lu, Q Mahmood, P Zheng (2015). Acute toxicity assessment of ANAMMOX substrates and antibiotics by luminescent bacteria test. Chemosphere, 140: 174–183
https://doi.org/10.1016/j.chemosphere.2015.03.057
23 J Du, W Qi, Q Niu, Y Hu, Y Zhang, M Yang, Y Y Li (2016). Inhibition and acclimation of nitrifiers exposed to erythromycin. Ecological Engineering, 94: 337–343
https://doi.org/10.1016/j.ecoleng.2016.06.006
24 L Du, S Cheng, Y Hou, X Sun, D Zhou, B Liu (2018). Influence of sulfadimethoxine (SDM) and sulfamethazine (SM) on anammox bioreactors: Performance evaluation and bacterial community characterization. Bioresource Technology, 267: 84–92
https://doi.org/10.1016/j.biortech.2018.05.067
25 N S Fan, X L Zhu, J Wu, Z Tian, Y H Bai, B C Huang, R C Jin (2019). Deciphering the microbial and genetic responses of anammox biogranules to the single and joint stress of zinc and tetracycline. Environment International, 132: 105097
https://doi.org/10.1016/j.envint.2019.105097
26 I Fernández, A Mosquera-Corral, J L Campos, R Méndez (2009). Operation of an Anammox SBR in the presence of two broad-spectrum antibiotics. Process Biochemistry, 44(4): 494–498
https://doi.org/10.1016/j.procbio.2009.01.001
27 F Gagné, C Blaise, C Andre (2006). Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicology and Environmental Safety, 64(3): 329–336
https://doi.org/10.1016/j.ecoenv.2005.04.004
28 P Gao, D Mao, Y Luo, L Wang, B Xu, L Xu (2012). Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, 46(7): 2355–2364
https://doi.org/10.1016/j.watres.2012.02.004
29 S Ghosh, T M LaPara (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME Journal, 1(3): 191–203
https://doi.org/10.1038/ismej.2007.31
30 C Gu, K G Karthikeyan, S D Sibley, J A Pedersen (2007). Complexation of the antibiotic tetracycline with humic acid. Chemosphere, 66(8): 1494–1501
https://doi.org/10.1016/j.chemosphere.2006.08.028
31 M T Guo, Q B Yuan, J Yang (2015a). Insights into the amplification of bacterial resistance to erythromycin in activated sludge. Chemosphere, 136: 79–85
https://doi.org/10.1016/j.chemosphere.2015.03.085
32 Q Guo, B S Xing, P Li, J L Xu, C C Yang, R C Jin (2015b). Anaerobic ammonium oxidation (anammox) under realistic seasonal temperature variations: Characteristics of biogranules and process performance. Bioresource Technology, 192: 765–773
https://doi.org/10.1016/j.biortech.2015.06.049
33 N Høiby , T Bjarnsholt, M Givskov, S Molin, O Ciofu (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35(4): 322–332
https://doi.org/10.1016/j.ijantimicag.2009.12.011
34 G Hou, X Hao, R Zhang, J Wang, R Liu, C Liu (2016). Tetracycline removal and effect on the formation and degradation of extracellular polymeric substances and volatile fatty acids in the process of hydrogen fermentation. Bioresource Technology, 212: 20–25
https://doi.org/10.1016/j.biortech.2016.03.156
35 Q Hu, X X Zhang, S Jia, K Huang, J Tang, P Shi, L Ye, H Ren (2016a). Metagenomic insights into ultraviolet disinfection effects on antibiotic resistome in biologically treated wastewater. Water Research, 101: 309–317
https://doi.org/10.1016/j.watres.2016.05.092
36 Z Hu, P Sun, Z Hu, J Han, R Wang, L Jiao, P Yang (2016b). Short-term performance of enhanced biological phosphorus removal (EBPR) system exposed to erythromycin (ERY) and oxytetracycline (OTC). Bioresource Technology, 221: 15–25
https://doi.org/10.1016/j.biortech.2016.08.102
37 Z Hu, T Van Alen, M S Jetten, B Kartal (2013). Lysozyme and penicillin inhibit the growth of anaerobic ammonium-oxidizing planctomycetes. Applied and Environmental Microbiology, 79(24): 7763–7769
https://doi.org/10.1128/AEM.02467-13
38 J Huang, Y Q Tang, J Y Sun (2010). Intravenous colistin sulfate: A rarely used form of polymyxin E for the treatment of severe multidrug-resistant gram-negative bacterial infections. Scandinavian Journal of Infectious Diseases, 42(4): 260–265
https://doi.org/10.3109/00365540903490018
39 L Huang, Y B Xu, J X Xu, J Y Ling, J L Chen, J L Zhou, L Zheng, Q P Du (2017). Antibiotic resistance genes (ARGs) in duck and fish production ponds with integrated or non-integrated mode. Chemosphere, 168: 1107–1114
https://doi.org/10.1016/j.chemosphere.2016.10.096
40 F Jia, Q Yang, X Liu, X Li, B Li, L Zhang, Y Peng (2017). Stratification of extracellular polymeric substances (EPS) for aggregated anammox microorganisms. Environmental Science & Technology, 51(6): 3260–3268
https://doi.org/10.1021/acs.est.6b05761
41 R C Jin, G F Yang, J J Yu, P Zheng (2012). The inhibition of the Anammox process: A review. Chemical Engineering Journal, 197: 67–79
https://doi.org/10.1016/j.cej.2012.05.014
42 R C Jin, Q Q Zhang, Z Z Zhang, J H Liu, B E Yang, L X Guo, H Z Wang (2014). Bio-augmentation for mitigating the impact of transient oxytetracycline shock on anaerobic ammonium oxidation (ANAMMOX) performance. Bioresource Technology, 163: 244–253
https://doi.org/10.1016/j.biortech.2014.04.029
43 S Johansson, M Ruscalleda, J Colprim (2017). Phosphorus recovery through biologically induced precipitation by partial nitritation-anammox granular biomass. Chemical Engineering Journal, 327: 881–888
https://doi.org/10.1016/j.cej.2017.06.129
44 B Kartal, W J Maalcke, N M de Almeida, I Cirpus, J Gloerich, W Geerts, H J Op Den Camp, H R Harhangi, E M Janssen-Megens, K J Francoijs, H G Stunnenberg, J T Keltjens, M S Jetten, M Strous (2011). Molecular mechanism of anaerobic ammonium oxidation. Nature, 479(7371): 127–130
https://doi.org/10.1038/nature10453
45 C Kunacheva, D C Stuckey (2014). Analytical methods for soluble microbial products (SMP) and extracellular polymers (ECP) in wastewater treatment systems: A review. Water Research, 61: 1–18
https://doi.org/10.1016/j.watres.2014.04.044
46 I Levin-Reisman, I Ronin, O Gefen, I Braniss, N Shoresh, N Q Balaban (2017). Antibiotic tolerance facilitates theevolution of resistance. Science, 355(6327): 826–830
https://doi.org/10.1126/science.aaj2191
47 Y Liang, D Li, X Zhang, H Zeng, J Zhang (2015). Performance and influence factors of completely autotrophic nitrogen removal over nitrite (CANON) process in a biofilter packed with volcanic rocks. Environmental Technology, 36(8): 946–952
https://doi.org/10.1080/09593330.2014.969327
48 J Lin, K Nishino, M C Roberts, M Tolmasky, R I Aminov, L Zhang (2015). Mechanisms of antibiotic resistance. Frontiers in Microbiology, 6: 1-3
https://doi.org/10.3389/fmicb.2015.00034
49 F Liu, G G Ying, R Tao, J L Zhao, J F Yang, L F Zhao (2009). Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environmental Pollution, 157(5): 1636–1642
https://doi.org/10.1016/j.envpol.2008.12.021
50 H Liu, Y Yang, H Sun, L Zhao, Y Liu (2018). Effect of tetracycline on microbial community structure associated with enhanced biological N&P removal in sequencing batch reactor. Bioresource Technology, 256: 414–420
https://doi.org/10.1016/j.biortech.2018.02.051
51 L Liu, V Gibson, X Huang, C Liu, G Zhu (2016). Effects of antibiotics on characteristics and microbial resistance of aerobic granules in sequencing batch reactors. Desalination and Water Treatment, 57(18): 8252–8261
https://doi.org/10.1080/19443994.2015.1024746
52 M Liu, Y Zhang, M Yang, Z Tian, L Ren, S Zhang (2012). Abundance and distribution of tetracycline resistance genes and mobile elements in an oxytetracycline production wastewater treatment system. Environmental Science & Technology, 46(14): 7551–7557
https://doi.org/10.1021/es301145m
53 T Lotti, M Cordola, R Kleerebezem, S Caffaz, C Lubello, M C Van Loosdrecht (2012). Inhibition effect of swine wastewater heavy metals and antibiotics on anammox activity. Water Science and Technology, 66(7): 1519–1526
https://doi.org/10.2166/wst.2012.344
54 B Ma, S Wang, S Cao, Y Miao, F Jia, R Du, Y Peng (2016). Biological nitrogen removal from sewage via anammox: Recent advances. Bioresource Technology, 200: 981–990
https://doi.org/10.1016/j.biortech.2015.10.074
55 J L Martinez, M B Sanchez, L Martinez-Solano, A Hernandez, L Garmendia, A Fajardo, C Alvarez-Ortega (2009). Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiology Reviews, 33(2): 430–449
https://doi.org/10.1111/j.1574-6976.2008.00157.x
56 D I Massé, N M Saady, Y Gilbert (2014). Potential of biological processes to eliminate antibiotics in livestock manure: An overview. Animals (Basel), 4(2): 146–163
https://doi.org/10.3390/ani4020146
57 Y Meng, B Sheng, F Meng (2019). Changes in nitrogen removal and microbiota of anammox biofilm reactors under tetracycline stress at environmentally and industrially relevant concentrations. Science of the Total Environment, 668: 379–388
https://doi.org/10.1016/j.scitotenv.2019.02.389
58 A Mulder, A A Graaf, L A Robertson, J G Kuenen (1995). Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiology Ecology, 16(3): 177–184
https://doi.org/10.1111/j.1574-6941.1995.tb00281.x
59 P L Noophan, P Narinhongtong, C Wantawin, J Munakata-Marr (2012). Effects of oxytetracycline on anammox activity. J Environ Sci Health A. Tox Hazard Subst Environ Eng, 47(6): 873–877
60 K Perron, O Caille, C Rossier, C Van Delden, J L Dumas, T Kohler (2004). CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. Journal of Biological Chemistry, 279(10): 8761–8768
https://doi.org/10.1074/jbc.M312080200
61 S Phanwilai, S Piyavorasakul, P L Noophan, K D Daniels, S A Snyder (2020). Inhibition of anaerobic ammonium oxidation (anammox) bacteria by addition of high and low concentrations of chloramphenicol and comparison of attached- and suspended-growth. Chemosphere, 238: 124570
https://doi.org/10.1016/j.chemosphere.2019.124570
62 Z Qiang, J J Macauley, M R Mormile, R Surampalli, C D Adams (2006). Treatment of Antibiotics and Antibiotic Resistant Bacteria in Swine Wastewater with Free Chlorine. Journal of Agricultural and Food Chemistry, 54(21): 8144–8154
https://doi.org/10.1021/jf060779h
63 J Qu, H Wang, K Wang, G Yu, B Ke, H Q Yu, H Ren, X Zheng, J Li, W W Li, S Gao, H Gong (2019). Municipal wastewater treatment in China: Development history and future perspectives. Frontiers of Environmental Science & Engineering, 13(6)
https://doi.org/10.1007/s11783-019-1172-x
64 M M Rahman, J Shan, P Yang, X Shang, Y Xia, X Yan (2018). Effects of long-term pig manure application on antibiotics, abundance of antibiotic resistance genes (ARGs), anammox and denitrification rates in paddy soils. Environmental Pollution, 240: 368–377
https://doi.org/10.1016/j.envpol.2018.04.135
65 A Rodriguez-Sanchez, A Margareto, T Robledo-Mahon, E Aranda, S Diaz-Cruz, J Gonzalez-Lopez, D Barcelo, R Vahala, A Gonzalez-Martinez (2017). Performance and bacterial community structure of a granular autotrophic nitrogen removal bioreactor amended with high antibiotic concentrations. Chemical Engineering Journal, 325: 257–269
https://doi.org/10.1016/j.cej.2017.05.078
66 M Gonzalez Ronquillo, J C Angeles Hernandez. (2017). Antibiotic and synthetic growth promoters in animal diets: Review of impact and analytical methods. Food Control, 72: 255–267
https://doi.org/10.1016/j.foodcont.2016.03.001
67 P Sabine Marie, T Pumpel, R Markt, S Murthy, C Bott, B Wett (2015). Comparative evaluation of multiple methods to quantify and characterise granular anammox biomass. Water Research, 68: 194–205
https://doi.org/10.1016/j.watres.2014.10.005
68 G P Sheng, H Q Yu, X Y Li (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: A review. Biotechnology Advances, 28(6): 882–894
https://doi.org/10.1016/j.biotechadv.2010.08.001
69 P Shi, S Jia, X X Zhang, T Zhang, S Cheng, A Li (2013). Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Research, 47(1): 111–120
https://doi.org/10.1016/j.watres.2012.09.046
70 Z J Shi, H Y Hu, Y Y Shen, J J Xu, M L Shi, R C Jin (2017). Long-term effects of oxytetracycline (OTC) on the granule-based anammox: Process performance and occurrence of antibiotic resistance genes. Biochemical Engineering Journal, 127: 110–118
https://doi.org/10.1016/j.bej.2017.08.009
71 R Singh, A P Singh, S Kumar, B S Giri, K H Kim (2019). Antibiotic resistance in major rivers in the world: A systematic review on occurrence, emergence, and management strategies. Journal of Cleaner Production, 234: 1484–1505
https://doi.org/10.1016/j.jclepro.2019.06.243
72 R H Song, X H Wang, G H Zhang, L Zhao, X F Sun, S G Wang, B Y Gao (2011). Simulation of equilibrium system and release behaviors of both oxytetracycline and copper on aerobic granules in a sequencing batch reactor. Biochemical Engineering Journal, 56(3): 198–204
https://doi.org/10.1016/j.bej.2011.06.009
73 M Strous, J J Heijnen, J G Kuenen, M S M Jetten (1998). The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Applied Microbiology and Biotechnology, 50(5): 589–596
https://doi.org/10.1007/s002530051340
74 R Suto, C Ishimoto, M Chikyu, Y Aihara, T Matsumoto, H Uenishi, T Yasuda, Y Fukumoto, M Waki (2017). Anammox biofilm in activated sludge swine wastewater treatment plants. Chemosphere, 167: 300–307
https://doi.org/10.1016/j.chemosphere.2016.09.121
75 C J Tang, P Zheng, C H Wang, Q Mahmood (2010). Suppression of anaerobic ammonium oxidizers under high organic content in high-rate anammox UASB reactor. Bioresource Technology, 101(6): 1762–1768
https://doi.org/10.1016/j.biortech.2009.10.032
76 C J Tang, P Zheng, C H Wang, Q Mahmood, J Q Zhang, X G Chen, L Zhang, J W Chen (2011). Performance of high-loaded anammox UASB reactors containing granular sludge. Water Research, 45(1): 135–144
https://doi.org/10.1016/j.watres.2010.08.018
77 Z Tian, Y Zhang, M Yang (2018). Chronic impacts of oxytetracycline on mesophilic anaerobic digestion of excess sludge: Inhibition of hydrolytic acidification and enrichment of antibiotic resistome. Environmental Pollution, 238: 1017–1026
https://doi.org/10.1016/j.envpol.2018.02.023
78 M Topal, E I Arslan Topal (2016). Determination and Monitoring of Tetracycline and Degradation Products in Landfill Leachate. Clean- Soil, Air. Water (Basel), 44(4): 444–450
79 Y Valcárcel, S González Alonso, J L Rodríguez-Gil, A Gil, M Catalá (2011). Detection of pharmaceutically active compounds in the rivers and tap water of the Madrid Region (Spain) and potential ecotoxicological risk. Chemosphere, 84(10): 1336–1348
https://doi.org/10.1016/j.chemosphere.2011.05.014
80 A A van de Graaf, P de Bruijn, L A Robertson, M S M Jetten, J G Kuenen (1996). Autotrophic growth of anaerobic ammonium-oxidizing micro-organismsin a fluidized bed reactor. Microbiology, 142(8): 2187–2196
https://doi.org/10.1099/13500872-142-8-2187
81 A A van de Graaf, A Mulder, P de Bruijn, M S Jetten, L A Robertson, J G Kuenen (1995). Anaerobic oxidation of ammonium is a biologically mediated process. Applied and Environmental Microbiology, 61(4): 1246–1251
https://doi.org/10.1128/AEM.61.4.1246-1251.1995
82 K Wan, W Lin, S Zhu, S Zhang, X Yu (2020). Biofiltration and disinfection codetermine the bacterial antibiotic resistome in drinking water: A review and meta-analysis. Frontiers of Environmental Science & Engineering, 14(1): 10
https://doi.org/10.1007/s11783-019-1189-1
83 L Wang, W Ben, Y Li, C Liu, Z Qiang (2018). Behavior of tetracycline and macrolide antibiotics in activated sludge process and their subsequent removal during sludge reduction by ozone. Chemosphere, 206: 184–191
https://doi.org/10.1016/j.chemosphere.2018.04.180
84 M Wang, R Li, Q Zhao (2019a). Distribution and removal of antibiotic resistance genes during anaerobic sludge digestion with alkaline, thermal hydrolysis and ultrasonic pretreatments. Frontiers of Environmental Science & Engineering, 13(3): 43
https://doi.org/10.1007/s11783-019-1127-2
85 S Wang, X Ma, Y Wang, G Du, J H Tay, J Li (2019b). Piggery wastewater treatment by aerobic granular sludge: Granulation process and antibiotics and antibiotic-resistant bacteria removal and transport. Bioresource Technology, 273: 350–357
https://doi.org/10.1016/j.biortech.2018.11.023
86 Y Wang, X Ma, S Zhou, X Lin, B Ma, H D Park, Y Yan (2016). Expression of the nirS, hzsA, and hdh genes in response to nitrite shock and recovery in Candidatus Kuenenia stuttgartiensis. Environmental Science & Technology, 50(13): 6940–6947
https://doi.org/10.1021/acs.est.6b00546
87 J Wu, N FanS, Y Y Yu, Y J He, Y H Zhao, Q Zhang, B C Huang, R C Jin (2020). Insight into the microbial and genetic responses of anammox granules to spiramycin: Comparison between two different dosing strategies. Journal of Cleaner Production, 258: 120993
https://doi.org/10.1016/j.jclepro.2020.120993
88 B S Xing, R C Jin (2018). Inhibitory effects of heavy metals and antibiotics on nitrifying bacterial activities in mature partial nitritation. Chemosphere, 200: 437–445
https://doi.org/10.1016/j.chemosphere.2018.02.132
89 J Xu, G P Sheng, Y Ma, L F Wang, H Q Yu (2013). Roles of extracellular polymeric substances (EPS) in the migration and removal of sulfamethazine in activated sludge system. Water Research, 47(14): 5298–5306
https://doi.org/10.1016/j.watres.2013.06.009
90 J Xu, Y Xu, H Wang, C Guo, H Qiu, Y He, Y Zhang, X Li, W Meng (2015). Occurrence of antibiotics and antibiotic resistance genes in a sewage treatment plant and its effluent-receiving river. Chemosphere, 119: 1379–1385
https://doi.org/10.1016/j.chemosphere.2014.02.040
91 L Z J Xu, Z J Shi, Q Guo, Y H Bai, Y Y Shen, L Y Jin, Y H Zhao, J T Zhang, R C Jin (2019). Performance and microbial community responses of the partial nitration process to tetracycline and Zn(II). Separation and Purification Technology, 229: 115810
https://doi.org/10.1016/j.seppur.2019.115810
92 Y Xu, J Xu, D Mao, Y Luo (2017). Effect of the selective pressure of sub-lethal level of heavy metals on the fate and distribution of ARGs in the catchment scale. Environmental Pollution, 220(Pt B): 900–908
93 G F Yang, R C Jin (2012). The joint inhibitory effects of phenol, copper(II), oxytetracycline (OTC) and sulfide on anammox activity. Bioresource Technology, 126: 187–192
https://doi.org/10.1016/j.biortech.2012.09.023
94 G F Yang, Q Q Zhang, R C Jin (2013). Changes in the nitrogen removal performance and the properties of granular sludge in an Anammox system under oxytetracycline (OTC) stress. Bioresource Technology, 129: 65–71
https://doi.org/10.1016/j.biortech.2012.11.022
95 H Yao, H Li, J Xu, L Zuo (2018). Inhibitive effects of chlortetracycline on performance of the nitritation-anaerobic ammonium oxidation (anammox) process and strategies for recovery. Journal of Environmental Sciences (China), 70: 29–36
https://doi.org/10.1016/j.jes.2017.11.005
96 H Yin, G Li, X Chen, W Wang, P K Wong, H Zhao, T An (2020). Accelerated evolution of bacterial antibiotic resistance through early emerged stress responses driven by photocatalytic oxidation. Applied Catalysis B: Environmental, 269: 118829
https://doi.org/10.1016/j.apcatb.2020.118829
97 F Zhang, Y Peng, L Miao, Z Wang, S Wang, B Li (2017). A novel simultaneous partial nitrification anammox and denitrification (SNAD) with intermittent aeration for cost-effective nitrogen removal from mature landfill leachate. Chemical Engineering Journal, 313: 619–628
https://doi.org/10.1016/j.cej.2016.12.105
98 H Zhang, Y Jia, S K Khanal, H Lu, H Fang, Q Zhao (2018a). Understanding the role of extracellular polymeric substances on ciprofloxacin adsorption in aerobic sludge, anaerobic sludge, and sulfate-reducing bacteria sludge systems. Environmental Science & Technology, 52(11): 6476–6486
https://doi.org/10.1021/acs.est.8b00568
99 M Zhang, S Wang, B Ji, Y Liu (2019a). Towards mainstream deammonification of municipal wastewater: Partial nitrification-anammox versus partial denitrification-anammox. Science of the Total Environment, 692: 393–401
https://doi.org/10.1016/j.scitotenv.2019.07.293
100 Q Q Zhang, Y H Bai, J Wu, L Z Xu, W Q Zhu, G M Tian, P Zheng, X Y Xu, R C Jin (2019b). Microbial community evolution and fate of antibiotic resistance genes in anammox process under oxytetracycline and sulfamethoxazole stresses. Bioresource Technology, 293: 122096
https://doi.org/10.1016/j.biortech.2019.122096
101 Q Q Zhang, H Chen, J H Liu, B E Yang, W M Ni, R C Jin (2014). The robustness of ANAMMOX process under the transient oxytetracycline (OTC) shock. Bioresource Technology, 153: 39–46
https://doi.org/10.1016/j.biortech.2013.11.053
102 Q Q Zhang, G F Yang, K K Sun, G M Tian, R C Jin (2018b). Insights into the effects of bio-augmentation on the granule-based anammox process under continuous oxytetracycline stress: Performance and microflora structure. Chemical Engineering Journal, 348: 503–513
https://doi.org/10.1016/j.cej.2018.04.204
103 Q Q Zhang, Y H Zhao, C J Wang, Y H Bai, D Wu, J Wu, G M Tian, M L Shi, Q Mahmood, R C Jin (2019c). Expression of the nirS, hzsA, and hdh genes and antibiotic resistance genes in response to recovery of anammox process inhibited by oxytetracycline. Science of the Total Environment, 681: 56–65
https://doi.org/10.1016/j.scitotenv.2019.04.438
104 W Zhang, M H Huang, F F Qi, P Z Sun, S W Van Ginkel (2013). Effect of trace tetracycline concentrations on the structure of a microbial community and the development of tetracycline resistance genes in sequencing batch reactors. Bioresource Technology, 150: 9–14
https://doi.org/10.1016/j.biortech.2013.09.081
105 X Zhang, T Chen, J Zhang, H Zhang, S Zheng, Z Chen, Y Ma (2018c). Performance of the nitrogen removal, bioactivity and microbial community responded to elevated norfloxacin antibiotic in an anammox biofilm system. Chemosphere, 210: 1185–1192
https://doi.org/10.1016/j.chemosphere.2018.07.100
106 X Zhang, Z Chen, Y Ma, T Chen, J Zhang, H Zhang, S Zheng, J Jia (2019d). Impacts of erythromycin antibiotic on anammox process: Performance and microbial community structure. Biochemical Engineering Journal, 143: 1–8
https://doi.org/10.1016/j.bej.2018.12.005
107 X Zhang, Z Chen, Y Ma, N Zhang, Q Pang, X Xie, Y Li, J Jia (2019e). Response of anammox biofilm to antibiotics in trace concentration: Microbial activity, diversity and antibiotic resistance genes. Journal of Hazardous Materials, 367: 182–187
https://doi.org/10.1016/j.jhazmat.2018.12.082
108 X Zhang, Z Chen, N Zhang, Y Ma, Y Song, Y Li, H Zhang (2020). Resistance to copper oxide nanoparticle and oxytetracycline of partial nitrification sludge. Chemical Engineering Journal, 381: 122661
https://doi.org/10.1016/j.cej.2019.122661
109 Z Z Zhang, Y F Cheng, L Z Xu, Y H Bai, J J Xu, Z J Shi, Q Q Zhang, R C Jin (2018d). Transient disturbance of engineered ZnO nanoparticles enhances the resistance and resilience of anammox process in wastewater treatment. Science of the Total Environment, 622–623: 402–409
https://doi.org/10.1016/j.scitotenv.2017.12.016
110 Z Z Zhang, Q Q Zhang, Q Guo, Q Q Chen, X Y Jiang, R C Jin (2015). Anaerobic ammonium-oxidizing bacteria gain antibiotic resistance during long-term acclimatization. Bioresource Technology, 192: 756–764
https://doi.org/10.1016/j.biortech.2015.06.044
111 W Zhi, G Ji (2014). Quantitative response relationships between nitrogen transformation rates and nitrogen functional genes in a tidal flow constructed wetland under C/N ratio constraints. Water Research, 64: 32–41
https://doi.org/10.1016/j.watres.2014.06.035
112 Y Zhu, Y Wang, X Jiang, S Zhou, M Wu, M Pan, H Chen (2017). Microbial community compositional analysis for membrane bioreactor treating antibiotics containing wastewater. Chemical Engineering Journal, 325: 300–309
https://doi.org/10.1016/j.cej.2017.05.073
113 Y G Zhu, T A Johnson, J Q Su, M Qiao, G X Guo, R D Stedtfeld, S A Hashsham, J M Tiedje (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9): 3435–3440
https://doi.org/10.1073/pnas.1222743110
[1] Tao Liu, Yudong Song, Zhiqiang Shen, Yuexi Zhou. Inhibition character of crotonaldehyde manufacture wastewater on biological acidification[J]. Front. Environ. Sci. Eng., 2021, 15(6): 119-.
[2] Fei Xie, Bowei Zhao, Ying Cui, Xiao Ma, Xiao Zhang, Xiuping Yue. Reutilize tire in microbial fuel cell for enhancing the nitrogen removal of the anammox process coupled with iron-carbon micro-electrolysis[J]. Front. Environ. Sci. Eng., 2021, 15(6): 121-.
[3] Yuan Meng, Weiyi Liu, Heidelore Fiedler, Jinlan Zhang, Xinrui Wei, Xiaohui Liu, Meng Peng, Tingting Zhang. Fate and risk assessment of emerging contaminants in reclaimed water production processes[J]. Front. Environ. Sci. Eng., 2021, 15(5): 104-.
[4] Kangying Guo, Baoyu Gao, Jie Wang, Jingwen Pan, Qinyan Yue, Xing Xu. Flocculation behaviors of a novel papermaking sludge-based flocculant in practical printing and dyeing wastewater treatment[J]. Front. Environ. Sci. Eng., 2021, 15(5): 103-.
[5] Zhifei Ma, Huali Cao, Fengchun Lv, Yu Yang, Chen Chen, Tianxue Yang, Haixin Zheng, Daishe Wu. Preparation of nZVI embedded modified mesoporous carbon for catalytic persulfate to degradation of reactive black 5[J]. Front. Environ. Sci. Eng., 2021, 15(5): 98-.
[6] Qinxue Wen, Shuo Yang, Zhiqiang Chen. Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: Dynamics of microbial communities and evolution of resistance genes[J]. Front. Environ. Sci. Eng., 2021, 15(5): 94-.
[7] Xinshu Liu, Xiaoman Su, Sijie Tian, Yue Li, Rongfang Yuan. Mechanisms for simultaneous ozonation of sulfamethoxazole and natural organic matters in secondary effluent from sewage treatment plant[J]. Front. Environ. Sci. Eng., 2021, 15(4): 75-.
[8] Mariana Valdez-Castillo, Sonia Arriaga. Response of bioaerosol cells to photocatalytic inactivation with ZnO and TiO2 impregnated onto Perlite and Poraver carriers[J]. Front. Environ. Sci. Eng., 2021, 15(3): 43-.
[9] Pil Uthaug Rasmussen, Katrine Uhrbrand, Mette Damkjær Bartels, Helle Neustrup, Dorina Gabriela Karottki, Ute Bültmann, Anne Mette Madsen. Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the quality of infection hygiene in nursing homes[J]. Front. Environ. Sci. Eng., 2021, 15(3): 41-.
[10] Dongjie Shang, Jianfei Peng, Song Guo, Zhijun Wu, Min Hu. Secondary aerosol formation in winter haze over the Beijing-Tianjin-Hebei Region, China[J]. Front. Environ. Sci. Eng., 2021, 15(2): 34-.
[11] Guoliang Zhang, Liang Zhang, Xiaoyu Han, Shujun Zhang, Yongzhen Peng. Start-up of PN-anammox system under low inoculation quantity and its restoration after low-loading rate shock[J]. Front. Environ. Sci. Eng., 2021, 15(2): 32-.
[12] Shengjie Qiu, Jinjin Liu, Liang Zhang, Qiong Zhang, Yongzhen Peng. Sludge fermentation liquid addition attained advanced nitrogen removal in low C/N ratio municipal wastewater through short-cut nitrification-denitrification and partial anammox[J]. Front. Environ. Sci. Eng., 2021, 15(2): 26-.
[13] Huibin Guo, Ning Wang, Xiang Li. Antioxidative potential of metformin: Possible protective mechanism against generating OH radicals[J]. Front. Environ. Sci. Eng., 2021, 15(2): 21-.
[14] Jing Ding, Wanyi Seow, Jizhong Zhou, Raymond Jianxiong Zeng, Jun Gu, Yan Zhou. Effects of Fe(II) on anammox community activity and physiologic response[J]. Front. Environ. Sci. Eng., 2021, 15(1): 7-.
[15] Ying Cui, Feng Tan, Yan Wang, Suyu Ren, Jingwen Chen. Diffusive gradients in thin films using molecularly imprinted polymer binding gels for in situ measurements of antibiotics in urban wastewaters[J]. Front. Environ. Sci. Eng., 2020, 14(6): 111-.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed