Distribution and removal of antibiotic resistance genes during anaerobic sludge digestion with alkaline, thermal hydrolysis and ultrasonic pretreatments
Mengli Wang, Ruying Li(), Qing Zhao
School of Environmental Science and Engineering, Tianjin University, Tianjin 300350, China
Sludge digestion is critical to control the spread of ARGs from wastewater to soil.
Fate of ARGs in three pretreatment-AD processes was investigated.
UP was more efficient for ARGs removal than AP and THP in pretreatment-AD process.
The total ARGs concentration showed significant correlation with 16S rRNA gene.
The bacteria carrying ARGs could be mainly affiliated with Proteobacteria.
Sewage sludge in the wastewater treatment plants contains considerable amount of antibiotic resistance genes (ARGs). A few studies have reported that anaerobic digestion (AD) could successfully remove some ARGs from sewage sludge, but information on the fate of ARGs in sludge pretreatment-AD process is still very limited. In this study, three sludge pretreatment methods, including alkaline, thermal hydrolysis and ultrasonic pretreatments, were compared to investigate the distribution and removal of ARGs in the sludge pretreatment-AD process. Results showed that the ARGs removal efficiency of AD itself was approximately 50.77%, and if these three sludge pretreatments were applied, the total ARGs removal efficiency of the whole pretreatment-AD process could be improved up to 52.50%–75.07%. The ultrasonic pretreatment was more efficient than alkaline and thermal hydrolysis pretreatments. Although thermal hydrolysis reduced ARGs obviously, the total ARGs rebounded considerably after inoculation and were only removed slightly in the subsequent AD process. Furthermore, it was found that the total ARGs concentration significantly correlated with the amount of 16S rRNA gene during the pretreatment and AD processes, and the bacteria carrying ARGs could be mainly affiliated with Proteobacteria.
APHA (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. Washington, DC: APHA
2
B Berglund (2015). Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics. Infection Ecology & Epidemiology, 5(1): 28564 https://doi.org/10.3402/iee.v5.28564
pmid: 26356096
3
K Bondarczuk, A Markowicz, Z Piotrowska-Seget (2016). The urgent need for risk assessment on the antibiotic resistance spread via sewage sludge land application. Environment International, 87: 49–55 https://doi.org/10.1016/j.envint.2015.11.011
pmid: 26646979
4
W Calero-Cáceres, A Melgarejo, M Colomer-Lluch, C Stoll, F Lucena, J Jofre, M Muniesa (2014). Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions. Environmental Science & Technology, 48(13): 7602–7611 https://doi.org/10.1021/es501851s
pmid: 24873655
5
D L Diehl, T M LaPara (2010). Effect of temperature on the fate of genes encoding tetracycline resistance and the integrase of class 1 integrons within anaerobic and aerobic digesters treating municipal wastewater solids. Environmental Science & Technology, 44(23): 9128–9133 https://doi.org/10.1021/es102765a
pmid: 21058743
6
I S Henriques, F Fonseca, A Alves, M J Saavedra, A Correia (2006). Occurrence and diversity of integrons and beta-lactamase genes among ampicillin-resistant isolates from estuarine waters. Research in Microbiology, 157(10): 938–947 https://doi.org/10.1016/j.resmic.2006.09.003
pmid: 17125975
7
S Houtmeyers, J Degrève, K Willems, R Dewil, L Appels (2014). Comparing the influence of low power ultrasonic and microwave pre-treatments on the solubilisation and semi-continuous anaerobic digestion of waste activated sludge. Bioresource Technology, 171: 44–49 https://doi.org/10.1016/j.biortech.2014.08.029
pmid: 25189507
8
F Ju, B Li, L Ma, Y Wang, D Huang, T Zhang (2016). Antibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters. Water Research, 91: 1–10 https://doi.org/10.1016/j.watres.2015.11.071
pmid: 26773390
9
K L Jury, T Vancov, R M Stuetz, S J Khan (2010). Antibiotic resistance dissemination and sewage treatment plants. In: Méndez-Vilas A, ed. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Seville: Formatex Research Center, 509–519
O H Lowry, N J Rosebrough, A L Farr, R J Randall (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193(1): 265–275
pmid: 14907713
12
Y Ma, C A Wilson, J T Novak, R Riffat, S Aynur, S Murthy, A Pruden (2011). Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environmental Science & Technology, 45(18): 7855–7861 https://doi.org/10.1021/es200827t
pmid: 21815642
M Munir, K Wong, I Xagoraraki (2011). Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Research, 45(2): 681–693 https://doi.org/10.1016/j.watres.2010.08.033
pmid: 20850863
15
J Pei, H Yao, H Wang, J Ren, X Yu (2016). Comparison of ozone and thermal hydrolysis combined with anaerobic digestion for municipal and pharmaceutical waste sludge with tetracycline resistance genes. Water Research, 99: 122–128 https://doi.org/10.1016/j.watres.2016.04.058
pmid: 27151286
16
Y Sun, Y X Shen, P Liang, J Zhou, Y Yang, X Huang (2016). Multiple antibiotic resistance genes distribution in ten large-scale membrane bioreactors for municipal wastewater treatment. Bioresource Technology, 222: 100–106 https://doi.org/10.1016/j.biortech.2016.09.117
pmid: 27716561
17
J Tong, J Liu, X Zheng, J Zhang, X Ni, M Chen, Y Wei (2016). Fate of antibiotic resistance bacteria and genes during enhanced anaerobic digestion of sewage sludge by microwave pretreatment. Bioresource Technology, 217: 37–43 https://doi.org/10.1016/j.biortech.2016.02.130
pmid: 26970692
18
J Tong, X Lu, J Zhang, Q Sui, R Wang, M Chen, Y Wei (2017). Occurrence of antibiotic resistance genes and mobile genetic elements in enterococci and genomic DNA during anaerobic digestion of pharmaceutical waste sludge with different pretreatments. Bioresource Technology, 235: 316–324 https://doi.org/10.1016/j.biortech.2017.03.104
pmid: 28371770
19
M C Williams, J R Wenner, I Rouzina, V A Bloomfield (2001). Effect of pH on the overstretching transition of double-stranded DNA: Evidence of force-induced DNA melting. Biophysical Journal, 80(2): 874–881 https://doi.org/10.1016/S0006-3495(01)76066-3
pmid: 11159454
20
C A Wilson, C T Tanneru, S Banjade, S N Murthy, J T Novak (2011). Anaerobic digestion of raw and thermally hydrolyzed wastewater solids under various operational conditions. Water Environment Research, 83(9): 815–825 https://doi.org/10.2175/106143011X12928814444934
pmid: 22073729
21
Y Wu, E Cui, Y Zuo, W Cheng, C Rensing, H Chen (2016). Influence of two-phase anaerobic digestion on fate of selected antibiotic resistance genes and class I integrons in municipal wastewater sludge. Bioresource Technology, 211: 414–421 https://doi.org/10.1016/j.biortech.2016.03.086
pmid: 27035472
22
B Zhang, M Ji, F Wang, R Li, K Zhang, X Yin, Q Li (2017). Damage of EPS and cell structures and improvement of high-solid anaerobic digestion of sewage sludge by combined (Ca(OH)2+ multiple-transducer ultrasonic) pretreatment. RSC Advances, 7(37): 22706–22714 https://doi.org/10.1039/C7RA01060E
23
J Zhang, M Chen, Q Sui, R Wang, J Tong, Y Wei (2016a). Fate of antibiotic resistance genes and its drivers during anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment. Bioresource Technology, 217: 28–36 https://doi.org/10.1016/j.biortech.2016.02.140
pmid: 26988135
24
J Zhang, C Lv, J Tong, J Liu, J Liu, D Yu, Y Wang, M Chen, Y Wei (2016b). Optimization and microbial community analysis of anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment. Bioresource Technology, 200: 253–261 https://doi.org/10.1016/j.biortech.2015.10.037
pmid: 26496214
25
T Zhang, Y Yang, A Pruden (2015). Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Applied Microbiology and Biotechnology, 99(18): 7771–7779 https://doi.org/10.1007/s00253-015-6688-9
pmid: 25994259
26
T Zhang, M Zhang, X Zhang, H H P Fang (2009). Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environmental Science & Technology, 43(10): 3455–3460 https://doi.org/10.1021/es803309m
pmid: 19544839
27
Q Zhao, R Li, M Ji, Z J Ren (2016). Organic content influences sediment microbial fuel cell performance and community structure. Bioresource Technology, 220: 549–556 https://doi.org/10.1016/j.biortech.2016.09.005
pmid: 27619708
28
G Zhen, X Lu, H Kato, Y Zhao, Y Y Li (2017). Overview of pretreatment strategies for enhancing sewage sludge disintegration and subsequent anaerobic digestion: Current advances, full-scale application and future perspectives. Renewable & Sustainable Energy Reviews, 69: 559–577 https://doi.org/10.1016/j.rser.2016.11.187
