Evaluating the impact of sulfamethoxazole on hydrogen production during dark anaerobic sludge fermentation

doi:10.1007/s11783-023-1607-2

Front. Environ. Sci. Eng.

2023, Vol. 17

Issue (1) : 7 https://doi.org/10.1007/s11783-023-1607-2

RESEARCH ARTICLE

Evaluating the impact of sulfamethoxazole on hydrogen production during dark anaerobic sludge fermentation

Tingting Zhu, Zhongxian Su, Wenxia Lai, Jiazeng Ding, Yufen Wang, Yingxin Zhao, Yiwen Liu(

)

School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, China

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Abstract

● SMX promotes hydrogen production from dark anaerobic sludge fermentation.

● SMX significantly enhances the hydrolysis and acidification processes.

● SMX suppresses the methanogenesis process in order to reduce hydrogen consumption.

● SMX enhances the relative abundance of hydrogen-VFAs producers.

● SMX brings possible environmental risks due to the enrichment of ARGs.

The impact of antibiotics on the environmental protection and sludge treatment fields has been widely studied. The recovery of hydrogen from waste activated sludge (WAS) has become an issue of great interest. Nevertheless, few studies have focused on the impact of antibiotics present in WAS on hydrogen production during dark anaerobic fermentation. To explore the mechanisms, sulfamethoxazole (SMX) was chosen as a representative antibiotic to evaluate how SMX influenced hydrogen production during dark anaerobic fermentation of WAS. The results demonstrated SMX promoted hydrogen production. With increasing additions of SMX from 0 to 500 mg/kg TSS, the cumulative hydrogen production elevated from 8.07 ± 0.37 to 11.89 ± 0.19 mL/g VSS. A modified Gompertz model further verified that both the maximum potential of hydrogen production (P_m) and the maximum rate of hydrogen production (R_m) were promoted. SMX did not affected sludge solubilization, but promoted hydrolysis and acidification processes to produce more hydrogen. Moreover, the methanogenesis process was inhibited so that hydrogen consumption was reduced. Microbial community analysis further demonstrated that the introduction of SMX improved the abundance of hydrolysis bacteria and hydrogen-volatile fatty acids (VFAs) producers. SMX synergistically influenced hydrolysis, acidification and acetogenesis to facilitate the hydrogen production.

Keywords Sulfamethoxazole Hydrogen production Dark anaerobic fermentation Waste activated sludge

Corresponding Author(s): Yiwen Liu

Issue Date: 01 August 2022

Cite this article:

Tingting Zhu,Zhongxian Su,Wenxia Lai, et al. Evaluating the impact of sulfamethoxazole on hydrogen production during dark anaerobic sludge fermentation[J]. Front. Environ. Sci. Eng., 2023, 17(1): 7.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-023-1607-2
https://academic.hep.com.cn/fese/EN/Y2023/V17/I1/7

Fig.1 Cumulative hydrogen production from anaerobic dark fermentation of WAS with the increase of SMX concentrations (A), maximum potential (B) and maximum rate (C) of hydrogen production by model simulation, in which symbols represent experimental data and lines represent model simulation.

Tab.1 Estimated P_m and R_m with the increase of SMX concentrations using Gompertz equation

Fig.2 The soluble protein and soluble carbohydrate concentrations (A), and the soluble COD concentrations (B) during sludge solubilization process with the increase of SMX concentrations.

Fig.3 Impact of SMX on hydrogen yield steps during anaerobic sludge fermentation: (A) the degradation of BSA for hydrolysis step during series II, (B) the VFAs production from glucose for acidification step during series III, (C) the degradation of butyrate for acetogenesis step during series IV, and (D) the degradation of acetate for methanogenesis step during series V.

Fig.4 The inhibition constant (A) and related enzyme activities (B) of four involved hydrogen production steps with the increase of SMX concentrations. Hydrolysis, acidification, acetogenesis and methanogenesis experiments were conducted by series II, III, IV and V.

Tab.2 The effect of SMX on the diversity of microorganisms

Fig.5 Effect of SMX on relative abundance of microorganisms at phylum (A) and genus (B) level.

1	P M Budiman, T Y Wu. (2018). Role of chemicals addition in affecting biohydrogen production through photofermentation. Energy Conversion and Management, 165 : 509– 527 https://doi.org/10.1016/j.enconman.2018.01.058
2	M Cai, J Liu, Y Wei. (2004). Enhanced biohydrogen production from sewage sludge with alkaline pretreatment. Environmental Science & Technology, 38( 11): 3195– 3202 https://doi.org/10.1021/es0349204 pmid: 15224755
3	H Chen, X Zeng, Y Zhou, X Yang, S S Lam, D Wang. (2020). Influence of roxithromycin as antibiotic residue on volatile fatty acids recovery in anaerobic fermentation of waste activated sludge. Journal of Hazardous Materials, 394 : 122570– 122580 https://doi.org/10.1016/j.jhazmat.2020.122570 pmid: 32244145
4	Y Gao, J Zhao, C Qin, Q Yuan, J Zhu, Y Sun, C Lu. (2021). Evaluating the effect of fluoxetine on mesophilic anaerobic dark biohydrogen fermentation of excess sludge. Bioresource Technology, 336 : 125320 https://doi.org/10.1016/j.biortech.2021.125320 pmid: 34034011
5	S Hahnke, T Langer, M Klocke ( 2018). Proteiniborus indolifex sp. nov., isolated from a thermophilic industrial-scale biogas plant. International Journal of Systematic and Evolutionary Microbiology, 68( 3): 824– 828 https://doi.org/10.1099/ijsem.0.002591 pmid: 29458500
6	J Hu, J Zhao, D Wang, X Li, D Zhang, Q Xu, L Peng, Q Yang, G Zeng. (2018a). Effect of diclofenac on the production of volatile fatty acids from anaerobic fermentation of waste activated sludge. Bioresource Technology, 254 : 7– 15 https://doi.org/10.1016/j.biortech.2018.01.059 pmid: 29413941
7	C Huang, Z Tang, B Xi, W Tan, W Guo, W Wu, C Ma. (2021). Environmental effects and risk control of antibiotic resistance genes in the organic solid waste aerobic composting system: a review. Frontiers of Environmental Science & Engineering, 15( 6): 127
8	P Izadi, U Schröder. (2022). What is the role of individual species within bidirectional electroactive microbial biofilms: A case study on Desulfarculus baarsii and Desulfurivibrio alkaliphilus. ChemElectroChem, 9( 2): 202101116– 202101125 https://doi.org/10.1002/celc.202101116
9	R Kristiansen, H T Nguyen, A M Saunders, J L Nielsen, R Wimmer, V Q Le, S J McIlroy, S Petrovski, R J Seviour, A Calteau, K L Nielsen, P H Nielsen. (2013). A metabolic model for members of the genus Tetrasphaera involved in enhanced biological phosphorus removal. ISME Journal, 7( 3): 543– 554 https://doi.org/10.1038/ismej.2012.136 pmid: 23178666
10	X Li, K Sui, J Zhang, X Liu, Q Xu, D Wang, Q Yang ( 2022). Revealing the mechanisms of rhamnolipid enhanced hydrogen production from dark fermentation of waste activated sludge. Science of the Total Environment, 806( Pt 1): 150347 https://doi.org/10.1016/j.scitotenv.2021.150347 pmid: 34563898
11	L Lu, D Xing, N Ren. (2012). Pyrosequencing reveals highly diverse microbial communities in microbial electrolysis cells involved in enhanced H2 production from waste activated sludge. Water Research, 46( 7): 2425– 2434 https://doi.org/10.1016/j.watres.2012.02.005 pmid: 22374298
12	A S Oberoi, Y Jia, H Zhang, S K Khanal, H Lu. (2019). Insights into the fate and removal of antibiotics in engineered biological treatment systems: a critical review. Environmental Science & Technology, 53( 13): 7234– 7264 https://doi.org/10.1021/acs.est.9b01131 pmid: 31244081
13	N Qi, X Hu, X Zhao, L Li, J Yang, Y Zhao, X Li. (2018). Fermentative hydrogen production with peanut shell as supplementary substrate: effects of initial substrate, pH and inoculation proportion. Renewable Energy, 127 : 559– 564 https://doi.org/10.1016/j.renene.2018.05.018
14	T Schmidt, B K McCabe, P W Harris, S Lee. (2018). Effect of trace element addition and increasing organic loading rates on the anaerobic digestion of cattle slaughterhouse wastewater. Bioresource Technology, 264 : 51– 57 https://doi.org/10.1016/j.biortech.2018.05.050 pmid: 29783131
15	C Tong, D Xiao, L Xie, J Yang, R Zhao, J Hao, Z Huo, Z Zeng, W Xiong. (2022). Swine manure facilitates the spread of antibiotic resistome including tigecycline-resistant tet(X) variants to farm workers and receiving environment. Science of the Total Environment, 808 : 152157– 152168 https://doi.org/10.1016/j.scitotenv.2021.152157 pmid: 34871697
16	B Wang, S Q Ji, X X Tian, L Y Qu, F L Li ( 2015). Brassicibacter thermophilus sp. nov., a thermophilic bacterium isolated from coastal sediment. International Journal of Systematic and Evolutionary Microbiology, 65( 9): 2870– 2874 https://doi.org/10.1099/ijs.0.000348 pmid: 25999591
17	D Wang, Y Duan, Q Yang, Y Liu, B J Ni, Q Wang, G Zeng, X Li, Z Yuan. (2018a). Free ammonia enhances dark fermentative hydrogen production from waste activated sludge. Water Research, 133 : 272– 281 https://doi.org/10.1016/j.watres.2018.01.051 pmid: 29407708
18	D Wang, B Liu, X Liu, Q Xu, Q Yang, Y Liu, G Zeng, X Li, B J Ni. (2018b). How does free ammonia-based sludge pretreatment improve methane production from anaerobic digestion of waste activated sludge. Chemosphere, 206 : 491– 501 https://doi.org/10.1016/j.chemosphere.2018.05.059 pmid: 29778074
19	D Wang, K Shuai, Q Xu, X Liu, Y Li, Y Liu, Q Wang, X Li, G Zeng, Q Yang. (2018c). Enhanced short-chain fatty acids production from waste activated sludge by combining calcium peroxide with free ammonia pretreatment. Bioresource Technology, 262 : 114– 123 https://doi.org/10.1016/j.biortech.2018.04.081 pmid: 29702420
20	G Wang, Z Jin, X Wang, T S George, G Feng, L Zhang. (2022a). Simulated root exudates stimulate the abundance of Saccharimonadales to improve the alkaline phosphatase activity in maize rhizosphere. Applied Soil Ecology, 170 : 104274– 104284 https://doi.org/10.1016/j.apsoil.2021.104274
21	H Wang, W Guo, R Yin, J Du, Q Wu, H Luo, B Liu, F Sseguya, N Ren. (2019a). Biochar-induced Fe(III) reduction for persulfate activation in sulfamethoxazole degradation: insight into the electron transfer, radical oxidation and degradation pathways. Chemical Engineering Journal, 362 : 561– 569 https://doi.org/10.1016/j.cej.2019.01.053
22	L Wang, C Yang, S Thangavel, Z Guo, C Chen, A Wang, W Liu. (2021). Enhanced hydrogen production in microbial electrolysis through strategies of carbon recovery from alkaline/thermal treated sludge. Frontiers of Environmental Science & Engineering, 15( 4): 56
23	Y Wang, D Wang, F Chen, Q Yang, Y Li, X Li, G Zeng. (2019b). Effect of triclocarban on hydrogen production from dark fermentation of waste activated sludge. Bioresource Technology, 279 : 307– 316 https://doi.org/10.1016/j.biortech.2019.02.016 pmid: 30739014
24	Y Wang, K Zheng, H Guo, Y Tong, T Zhu, Y Liu. (2022b). Unveiling the mechanisms of how vivianite affects anaerobic digestion of waste activated sludge. Bioresource Technology, 343 : 126045 https://doi.org/10.1016/j.biortech.2021.126045 pmid: 34592460
25	Y Wei, A Zhou, Y Duan, Z Liu, Z He, J Zhang, B Liang, X Yue. (2022). Unraveling the behaviors of sulfonamide antibiotics on the production of short-chain fatty acids by anaerobic fermentation from waste activated sludge and the microbial ecological mechanism. Chemosphere, 296 : 133903– 133911 https://doi.org/10.1016/j.chemosphere.2022.133903 pmid: 35149007
26	S L Wu, G Luo, J Sun, W Wei, L Song, B J Ni. (2021). Medium chain fatty acids production from anaerobic fermentation of waste activated sludge. Journal of Cleaner Production, 279 : 123482– 123492 https://doi.org/10.1016/j.jclepro.2020.123482
27	Y Wu, D Wang, X Liu, Q Xu, Y Chen, Q Yang, H Li, B Ni. (2019). Effect of poly aluminum chloride on dark fermentative hydrogen accumulation from waste activated sludge. Water Research, 153 : 217– 228 https://doi.org/10.1016/j.watres.2019.01.016 pmid: 30721840
28	J Xie, X Duan, L Feng, Y Yan, F Wang, H Dong, R Jia, Q Zhou. (2019). Influence of sulfadiazine on anaerobic fermentation of waste activated sludge for volatile fatty acids production: Focusing on microbial responses. Chemosphere, 219 : 305– 312 https://doi.org/10.1016/j.chemosphere.2018.12.015 pmid: 30543966
29	T Yan, Q Yang, R Feng, X Ren, Y Zhao, M Sun, L Yan, Q Wei. (2022). Highly effective visible-photocatalytic hydrogen evolution and simultaneous organic pollutant degradation over an urchin-like oxygen-doped MoS2/ZnIn2S4 composite. Frontiers of Environmental Science & Engineering, 16( 10): 131
30	G Yang, J Wang. (2021). Enhancing biohydrogen production from disintegrated sewage sludge by combined sodium citrate-thermal pretreatment. Journal of Cleaner Production, 312 : 127756– 127765 https://doi.org/10.1016/j.jclepro.2021.127756
31	L Yang, K Li, S Cui, Y Kang, L An, K Lei. (2019). Removal of microplastics in municipal sewage from China’s largest water reclamation plant. Water Research, 155 : 175– 181 https://doi.org/10.1016/j.watres.2019.02.046 pmid: 30849731
32	S Zeng, J Sun, Z Chen, Q Xu, W Wei, D Wang, B J Ni. (2021). The impact and fate of clarithromycin in anaerobic digestion of waste activated sludge for biogas production. Environmental Research, 195 : 110792 https://doi.org/10.1016/j.envres.2021.110792 pmid: 33545126
33	J Zhao, D Wang, Y Liu, H H Ngo, W Guo, Q Yang, X Li. (2018). Novel stepwise pH control strategy to improve short chain fatty acid production from sludge anaerobic fermentation. Bioresource Technology, 249 : 431– 438 https://doi.org/10.1016/j.biortech.2017.10.050 pmid: 29065325
34	Q Zhao, W Guo, H Luo, C Xing, H Wang, B Liu, Q Si, D Li, L Sun, N Ren. (2022). Insights into removal of sulfonamides in anaerobic activated sludge system: Mechanisms, degradation pathways and stress responses. Journal of Hazardous Materials, 423( B): 127248– 127261 https://doi.org/10.1016/j.jhazmat.2021.127248
35	Y Zhao, Y Chen, D Zhang, X Zhu. (2010). Waste activated sludge fermentation for hydrogen production enhanced by anaerobic process improvement and acetobacteria inhibition: the role of fermentation pH. Environmental Science & Technology, 44( 9): 3317– 3323 https://doi.org/10.1021/es902958c pmid: 20377173
36	T Zhu, Y Zhang, G Bu, X Quan, Y Liu. (2016). Producing nitrite from anodic ammonia oxidation to accelerate anammox in a bioelectrochemical system with a given anode potential. Chemical Engineering Journal, 291 : 184– 191 https://doi.org/10.1016/j.cej.2016.01.099
37	T T Zhu, H Y Cheng, L H Yang, S G Su, H C Wang, S S Wang, A J Wang. (2019). Coupled sulfur and iron(II) carbonate-driven autotrophic denitrification for significantly enhanced nitrate removal. Environmental Science & Technology, 53( 3): 1545– 1554 https://doi.org/10.1021/acs.est.8b06865 pmid: 30596484
38	T T Zhu, Z X Su, W X Lai, Y B Zhang, Y W Liu. (2021). Insights into the fate and removal of antibiotics and antibiotic resistance genes using biological wastewater treatment technology. Science of the Total Environment, 776 : 145906– 145922 https://doi.org/10.1016/j.scitotenv.2021.145906

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[11]	Dawei LIANG,Yanyan LIU,Sikan PENG,Fei LAN,Shanfu LU,Yan XIANG. Effects of bicarbonate and cathode potential on hydrogen production in a biocathode electrolysis cell[J]. Front.Environ.Sci.Eng., 2014, 8(4): 624-630.
[12]	Gefu ZHU, Chaoxiang LIU, Jianzheng LI, Nanqi REN, Lin LIU, Xu HUANG. Fermentative hydrogen production from beet sugar factory wastewater treatment in a continuous stirred tank reactor using anaerobic mixed consortia[J]. Front Envir Sci Eng, 2013, 7(1): 143-150.
[13]	Sheng CHANG, Jianzheng LI, Feng LIU, Ze YU. Effect of different gas releasing methods on anaerobic fermentative hydrogen production in batch cultures[J]. Front Envir Sci Eng, 2012, 6(6): 901-906.
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