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.    2019, Vol. 13 Issue (6) : 84    https://doi.org/10.1007/s11783-019-1168-6
RESEARCH ARTICLE
Anaerobic biodegradation of trimethoprim with sulfate as an electron acceptor
Bin Liang2, Deyong Kong1,2(), Mengyuan Qi3, Hui Yun4, Zhiling Li3, Ke Shi3, E Chen5, Alisa S. Vangnai6,7, Aijie Wang2,3()
1. Shenyang Academy of Environmental Sciences, Shenyang 110167, China
2. Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
3. State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China
4. Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou University, Lanzhou 730000, China
5. The Environmental Monitoring Center of Gansu Province, Lanzhou 730020, China
6. Department of Biochemistry, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand
7. Center of Excellence on Hazardous Substance Management (HSM), Chulalongkorn University, Bangkok 10330, Thailand
 Download: PDF(1379 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Anaerobic biodegradation of trimethoprim (TMP) coupled with sulfate reduction.

Demethylation of TMP is the first step in the acclimated microbial consortia.

The potential degraders and fermenters were enriched in the acclimated consortia.

Activated sludge and river sediment had similar core microbiomes.

Trimethoprim (TMP) is an antibiotic frequently detected in various environments. Microorganisms are the main drivers of emerging antibiotic contaminant degradation in the environment. However, the feasibility and stability of the anaerobic biodegradation of TMP with sulfate as an electron acceptor remain poorly understood. Here, TMP-degrading microbial consortia were successfully enriched from municipal activated sludge (AS) and river sediment (RS) as the initial inoculums. The acclimated consortia were capable of transforming TMP through demethylation, and the hydroxyl-substituted demethylated product (4-desmethyl-TMP) was further degraded. The biodegradation of TMP followed a 3-parameter sigmoid kinetic model. The potential degraders (Acetobacterium, Desulfovibrio, Desulfobulbus, and unidentified Peptococcaceae) and fermenters (Lentimicrobium and Petrimonas) were significantly enriched in the acclimated consortia. The AS- and RS-acclimated TMP-degrading consortia had similar core microbiomes. The anaerobic biodegradation of TMP could be coupled with sulfate respiration, which gives new insights into the antibiotic fate in real environments and provides a new route for the bioremediation of antibiotic-contaminated environments.

Keywords Trimethoprim (TMP) biodegradation      Demethylation      Sulfate reduction      Core microbiome      Antibiotic fate     
Corresponding Authors: Deyong Kong,Aijie Wang   
Issue Date: 15 November 2019
 Cite this article:   
Bin Liang,Deyong Kong,Mengyuan Qi, et al. Anaerobic biodegradation of trimethoprim with sulfate as an electron acceptor[J]. Front. Environ. Sci. Eng., 2019, 13(6): 84.
 URL:  
http://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1168-6
http://academic.hep.com.cn/fese/EN/Y2019/V13/I6/84
Fig.1  Anaerobic biodegradation of TMP coupled with sulfate respiration with AS (a) or RS (b) as the initial inoculum over eight generations.
Fig.2  Taxonomic identification of the TMP-degrading microbial communities at the phylum (a), class (b) and genus (c) levels.
Fig.3  Hierarchical clustering analysis of the identified genera in the TMP-degrading microbial communities with AS and RS as the initial inoculums.
Fig.4  Principal coordinate analysis (PCoA) of the identified OTUs from the AS- and RS-acclimated TMP-degrading microbial communities with sulfate as the electron acceptor.
1 T D Allen, P F Kraus, P A Lawson, G R Drake, D L Balkwill, R S Tanner (2008). Desulfovibrio carbinoliphilus sp. nov., a benzyl alcohol-oxidizing, sulfate-reducing bacterium isolated from a gas condensate-contaminated aquifer. International Journal of Systematic and Evolutionary Microbiology, 58(6): 1313–1317
https://doi.org/10.1099/ijs.0.65524-0 pmid: 18523171
2 R Bache, N Pfennig (1981). Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Archives of Microbiology, 130(3): 255–261
https://doi.org/10.1007/BF00459530
3 A L Batt, S Kim, D S Aga (2006). Enhanced biodegradation of iopromide and trimethoprim in nitrifying activated sludge. Environmental Science & Technology, 40(23): 7367–7373
https://doi.org/10.1021/es060835v pmid: 17180990
4 J Benner, D De Smet, A Ho, F M Kerckhof, L Vanhaecke, K Heylen, N Boon (2015). Exploring methane-oxidizing communities for the co-metabolic degradation of organic micropollutants. Applied Microbiology and Biotechnology, 99(8): 3609–3618
https://doi.org/10.1007/s00253-014-6226-1 pmid: 25487887
5 H Bouju, B Ricken, T Beffa, P F X Corvini, B A Kolvenbach (2012). Isolation of bacterial strains capable of sulfamethoxazole mineralization from an acclimated membrane bioreactor. Applied and Environmental Microbiology, 78(1): 277–279
https://doi.org/10.1128/AEM.05888-11 pmid: 22020509
6 Z Cetecioglu, B Ince, D Orhon, O Ince (2016). Anaerobic sulfamethoxazole degradation is driven by homoacetogenesis coupled with hydrogenotrophic methanogenesis. Water Research, 90: 79–89
https://doi.org/10.1016/j.watres.2015.12.013 pmid: 26724442
7 F Chen, Z L Li, J Q Yang, B Liang, X Q Lin, J Nan, A J Wang (2018). Effects of different carbon substrates on performance, microbiome community structure and function for bioelectrochemical-stimulated dechlorination of tetrachloroethylene. Chemical Engineering Journal, 352: 730–736
https://doi.org/10.1016/j.cej.2018.07.082
8 T S Crofts, B Wang, A Spivak, T A Gianoulis, K J Forsberg, M K Gibson, L A Johnsky, S M Broomall, C N Rosenzweig, E W Skowronski, H S Gibbons, M O A Sommer, G Dantas (2018). Shared strategies for β-lactam catabolism in the soil microbiome. Nature Chemical Biology, 14(6): 556–564
pmid: 29713061
9 M Daghio, E Vaiopoulou, S A Patil, A Suárez-Suárez, I M Head, A Franzetti, K Rabaey (2016). Anodes stimulate anaerobic toluene degradation via sulfur cycling in marine sediments. Applied and Environmental Microbiology, 82(1): 297–307
https://doi.org/10.1128/AEM.02250-15 pmid: 26497463
10 Y Deng, B Li, T Zhang (2018a). Bacteria that make a meal of sulfonamide antibiotics: Blind spots and emerging opportunities. Environmental Science & Technology, 52(7): 3854–3868
https://doi.org/10.1021/acs.est.7b06026 pmid: 29498514
11 Y Deng, Y Mao, B Li, C Yang, T Zhang (2016). Aerobic degradation of sulfadiazine by Arthrobacter spp.: Kinetics, pathways, and genomic characterization. Environmental Science & Technology, 50(17): 9566–9575
https://doi.org/10.1021/acs.est.6b02231 pmid: 27477918
12 Y Deng, Y Wang, Y Mao, T Zhang (2018b). Partnership of Arthrobacter and Pimelobacter in aerobic degradation of sulfadiazine revealed by metagenomics analysis and isolation. Environmental Science & Technology, 52(5): 2963–2972
https://doi.org/10.1021/acs.est.7b05913 pmid: 29378398
13 A Grabowski, B J Tindall, V Bardin, D Blanchet, C Jeanthon (2005). Petrimonas sulfuriphila gen. nov., sp. nov., a mesophilic fermentative bacterium isolated from a biodegraded oil reservoir. International Journal of Systematic and Evolutionary Microbiology, 55(3): 1113–1121
https://doi.org/10.1099/ijs.0.63426-0 pmid: 15879242
14 M R Haider, W L Jiang, J L Han, H M A Sharif, Y C Ding, H Y Cheng, A J Wang (2019). In-situ electrode fabrication from polyaniline derived N-doped carbon nanofibers for metal-free electro-Fenton degradation of organic contaminants. Applied Catalysis B: Environmental, 256: 117774
https://doi.org/10.1016/j.apcatb.2019.117774
15 X Han, A C Scott, P M Fedorak, M Bataineh, J W Martin (2008). Influence of molecular structure on the biodegradability of naphthenic acids. Environmental Science & Technology, 42(4): 1290–1295
https://doi.org/10.1021/es702220c pmid: 18351107
16 L Huang, Q Wang, X Quan, Y Liu, G Chen (2013). Bioanodes/biocathodes formed at optimal potentials enhance subsequent pentachlorophenol degradation and power generation from microbial fuel cells. Bioelectrochemistry (Amsterdam, Netherlands), 94: 13–22
https://doi.org/10.1016/j.bioelechem.2013.05.001 pmid: 23747520
17 K S Jewell, S Castronovo, A Wick, P Falås, A Joss, T A Ternes (2016). New insights into the transformation of trimethoprim during biological wastewater treatment. Water Research, 88: 550–557
https://doi.org/10.1016/j.watres.2015.10.026 pmid: 26546758
18 Y Jia, S K Khanal, H Shu, H Zhang, G H Chen, H Lu (2018). Ciprofloxacin degradation in anaerobic sulfate-reducing bacteria (SRB) sludge system: Mechanism and pathways. Water Research, 136: 64–74
https://doi.org/10.1016/j.watres.2018.02.057 pmid: 29494897
19 Y Jia, S K Khanal, H Zhang, G H Chen, H Lu (2017). Sulfamethoxazole degradation in anaerobic sulfate-reducing bacteria sludge system. Water Research, 119: 12–20
https://doi.org/10.1016/j.watres.2017.04.040 pmid: 28433879
20 Y Jia, H Zhang, S K Khanal, L Yin, H Lu (2019). Insights into pharmaceuticals removal in an anaerobic sulfate-reducing bacteria sludge system. Water Research, 161: 191–201
https://doi.org/10.1016/j.watres.2019.06.010 pmid: 31195335
21 B Jiang, A Li, D Cui, R Cai, F Ma, Y Wang (2014). Biodegradation and metabolic pathway of sulfamethoxazole by Pseudomonas psychrophila HA-4, a newly isolated cold-adapted sulfamethoxazole-degrading bacterium. Applied Microbiology and Biotechnology, 98(10): 4671–4681
https://doi.org/10.1007/s00253-013-5488-3 pmid: 24522726
22 W L Jiang, X Xia, J L Han, Y C Ding, M R Haider, A J Wang (2018). Graphene modified electro-fenton catalytic membrane for in situ degradation of antibiotic florfenicol. Environmental Science & Technology, 52(17): 9972–9982
https://doi.org/10.1021/acs.est.8b01894 pmid: 30067345
23 E Kassotaki, G Buttiglieri, L Ferrando-Climent, I Rodriguez-Roda, M Pijuan (2016). Enhanced sulfamethoxazole degradation through ammonia oxidizing bacteria co-metabolism and fate of transformation products. Water Research, 94: 111–119
https://doi.org/10.1016/j.watres.2016.02.022 pmid: 26938496
24 R Kleemann, R U Meckenstock (2011). Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiology Ecology, 78(3): 488–496
https://doi.org/10.1111/j.1574-6941.2011.01193.x pmid: 22066721
25 D Kong, B Liang, H Yun, H Cheng, J Ma, M Cui, A Wang, N Ren (2015). Cathodic degradation of antibiotics: characterization and pathway analysis. Water Research, 72: 281–292
https://doi.org/10.1016/j.watres.2015.01.025 pmid: 25660806
26 D Li, R Qi, M Yang, Y Zhang, T Yu (2011). Bacterial community characteristics under long-term antibiotic selection pressures. Water Research, 45(18): 6063–6073
https://doi.org/10.1016/j.watres.2011.09.002 pmid: 21937072
27 B Liang, H Cheng, J D Van Nostrand, J Ma, H Yu, D Kong, W Liu, N Ren, L Wu, A Wang, D J Lee, J Zhou (2014). Microbial community structure and function of nitrobenzene reduction biocathode in response to carbon source switchover. Water Research, 54: 137–148
https://doi.org/10.1016/j.watres.2014.01.052 pmid: 24565804
28 B Liang, H Y Cheng, D Y Kong, S H Gao, F Sun, D Cui, F Y Kong, A J Zhou, W Z Liu, N Q Ren, W M Wu, A J Wang, D J Lee (2013). Accelerated reduction of chlorinated nitroaromatic antibiotic chloramphenicol by biocathode. Environmental Science & Technology, 47(10): 5353–5361
https://doi.org/10.1021/es400933h pmid: 23607616
29 B Liang, J Ma, W Cai, Z Li, W Liu, M Qi, Y Zhao, X Ma, Y Deng, A Wang, J Zhou (2019). Response of chloramphenicol-reducing biocathode resistome to continuous electrical stimulation. Water Research, 148: 398–406
https://doi.org/10.1016/j.watres.2018.10.073 pmid: 30399554
30 Q Liu, M Li, X Liu, Q Zhang, R Liu, Z Wang, X Shi, J Quan, X Shen, F Zhang (2018). Removal of sulfamethoxazole and trimethoprim from reclaimed water and the biodegradation mechanism. Frontiers of Environmental Science & Engineering, 12(6): 6
31 Y Luo, W Guo, H H Ngo, L D Nghiem, F I Hai, J Zhang, S Liang, X C C Wang (2014). A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Science of the Total Environment, 473–474: 619–641
https://doi.org/10.1016/j.scitotenv.2013.12.065 pmid: 24394371
32 X Ma, M Qi, Z Li, Y Zhao, P Yan, B Liang, A Wang (2019). Characterization of an efficient chloramphenicol-mineralizing bacterial consortium. Chemosphere, 222: 149–155
pmid: 30703654
33 L J Pan, X D Tang, C X Li, G W Yu, Y Wang (2017). Biodegradation of sulfamethazine by an isolated thermophile-Geobacillus sp. S-07. World Journal of Microbiology & Biotechnology, 33(5): 85
https://doi.org/10.1007/s11274-017-2245-2 pmid: 28378223
34 L Q Qiu, L Zhang, K Tang, G Chen, S Kumar Khanal, H Lu (2019). Removal of sulfamethoxazole (SMX) in sulfate-reducing flocculent and granular sludge systems. Bioresource Technology, 288: 121592
https://doi.org/10.1016/j.biortech.2019.121592 pmid: 31176940
35 K Rasool, S H Woo, D S Lee (2013). Simultaneous removal of COD and Direct Red 80 in a mixed anaerobic sulfate-reducing bacteria culture. Chemical Engineering Journal, 223: 611–616
https://doi.org/10.1016/j.cej.2013.03.031
36 W Reichenbecher, B Schink (1997). Desulfovibrio inopinatus, sp. nov., a new sulfate-reducing bacterium that degrades hydroxyhydroquinone (1,2,4-trihydroxybenzene). Archives of Microbiology, 168(4): 338–344
https://doi.org/10.1007/s002030050507 pmid: 9297472
37 X Song, R Liu, L Chen, T Kawagishi (2017). Comparative experiment on treating digested piggery wastewater with a biofilm MBR and conventional MBR: Simultaneous removal of nitrogen and antibiotics. Frontiers of Environmental Science & Engineering, 11(2): 11
38 L Sun, M Toyonaga, A Ohashi, D M Tourlousse, N Matsuura, X Y Meng, H Tamaki, S Hanada, R Cruz, T Yamaguchi, Y Sekiguchi (2016). Lentimicrobium saccharophilum gen. nov., sp. nov., a strictly anaerobic bacterium representing a new family in the phylum Bacteroidetes, and proposal of Lentimicrobiaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology, 66(7): 2635–2642
https://doi.org/10.1099/ijsem.0.001103 pmid: 27098854
39 T P Van Boeckel, C Brower, M Gilbert, B T Grenfell, S A Levin, T P Robinson, A Teillant, R Laxminarayan (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences of the United States of America, 112(18): 5649–5654
https://doi.org/10.1073/pnas.1503141112 pmid: 25792457
40 B M van der Zaan, F T Saia, A J Stams, C M Plugge, W M de Vos, H Smidt, A A Langenhoff, J Gerritse (2012). Anaerobic benzene degradation under denitrifying conditions: Peptococcaceae as dominant benzene degraders and evidence for a syntrophic process. Environmental Microbiology, 14(5): 1171–1181
https://doi.org/10.1111/j.1462-2920.2012.02697.x pmid: 22296107
41 L Wang, Y Liu, J Ma, F Zhao (2016). Rapid degradation of sulphamethoxazole and the further transformation of 3-amino-5-methylisoxazole in a microbial fuel cell. Water Research, 88: 322–328
https://doi.org/10.1016/j.watres.2015.10.030 pmid: 26512810
42 H Wu, Q Sun, Y Sun, Y Zhou, J Wang, C Hou, X Jiang, X Liu, J Shen (2019). Co-metabolic enhancement of 1H-1,2,4-triazole biodegradation through nitrification. Bioresource Technology, 271: 236–243
https://doi.org/10.1016/j.biortech.2018.09.112 pmid: 30273827
43 X Xu, R Zarecki, S Medina, S Ofaim, X Liu, C Chen, S Hu, D Brom, D Gat, S Porob, H Eizenberg, Z Ronen, J Jiang, S Freilich (2019). Modeling microbial communities from atrazine contaminated soils promotes the development of biostimulation solutions. The ISME Journal, 13(2): 494–508
https://doi.org/10.1038/s41396-018-0288-5 pmid: 30291327
44 L Yang, G Yi, Y Hou, H Cheng, X Luo, S G Pavlostathis, S Luo, A Wang (2019). Building electrode with three-dimensional macroporous interface from biocompatible polypyrrole and conductive graphene nanosheets to achieve highly efficient microbial electrocatalysis. Biosensors & Bioelectronics, 141: 111444
https://doi.org/10.1016/j.bios.2019.111444 pmid: 31226603
45 Y Yuan, C Chen, B Liang, C Huang, Y Zhao, X Xu, W Tan, X Zhou, S Gao, D Sun, D Lee, J Zhou, A Wang (2014). Fine-tuning key parameters of an integrated reactor system for the simultaneous removal of COD, sulfate and ammonium and elemental sulfur reclamation. Journal of Hazardous Materials, 269: 56–67
https://doi.org/10.1016/j.jhazmat.2013.12.014 pmid: 24373982
46 H Yun, D Kong, B Liang, M Cui, Z Li, A Wang (2016). Response of anodic bacterial community to the polarity inversion for chloramphenicol reduction. Bioresource Technology, 221: 666–670
https://doi.org/10.1016/j.biortech.2016.09.047 pmid: 27664010
47 H Yun, B Liang, J Qiu, L Zhang, Y Zhao, J Jiang, A Wang (2017). Functional characterization of a novel amidase involved in biotransformation of triclocarban and its dehalogenated congeners in Ochrobactrum sp. TCC-2. Environmental Science & Technology, 51(1): 291–300
https://doi.org/10.1021/acs.est.6b04885 pmid: 27966913
48 G Zellner, H Kneifel, J Winter (1990). Oxidation of benzaldehydes to benzoic acid derivatives by three Desulfovibrio strains. Applied and Environmental Microbiology, 56(7): 2228–2233
pmid: 2389937
49 H Zhang, S K Khanal, Y Jia, S Song, H Lu (2019). Fundamental insights into ciprofloxacin adsorption by sulfate-reducing bacteria sludge: Mechanisms and thermodynamics. Chemical Engineering Journal, 378: 122103
https://doi.org/10.1016/j.cej.2019.122103
50 Q Q Zhang, G G Ying, C G Pan, Y S Liu, J L Zhao (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of China: Source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science & Technology, 49(11): 6772–6782
https://doi.org/10.1021/acs.est.5b00729 pmid: 25961663
51 Y Zhao, Y Bai, Q Guo, Z Li, M Qi, X Ma, H Wang, D Kong, A Wang, B Liang (2019). Bioremediation of contaminated urban river sediment with methanol stimulation: Metabolic processes accompanied with microbial community changes. Science of the Total Environment, 653: 649–657
https://doi.org/10.1016/j.scitotenv.2018.10.396 pmid: 30759590
52 Y Zhao, Z Li, J Ma, H Yun, M Qi, X Ma, H Wang, A Wang, B Liang (2018). Enhanced bioelectroremediation of a complexly contaminated river sediment through stimulating electroactive degraders with methanol supply. Journal of Hazardous Materials, 349: 168–176
https://doi.org/10.1016/j.jhazmat.2018.01.060 pmid: 29421353
53 J Zhou, Q He, C L Hemme, A Mukhopadhyay, K Hillesland, A Zhou, Z He, J D Van Nostrand, T C Hazen, D A Stahl, J D Wall, A P Arkin (2011). How sulphate-reducing microorganisms cope with stress: Lessons from systems biology. Nature Reviews. Microbiology, 9(6): 452–466
https://doi.org/10.1038/nrmicro2575 pmid: 21572460
[1] FSE-19087-OF-LB_suppl_1 Download
[1] Jun Li, Wentao Li, Gan Luo, Yan Li, Aimin Li. Effect of nitrobenzene on the performance and bacterial community in an expanded granular sludge bed reactor treating high-sulfate organic wastewater[J]. Front. Environ. Sci. Eng., 2019, 13(1): 6-.
[2] Yi Chen, Shilong He, Mengmeng Zhou, Tingting Pan, Yujia Xu, Yingxin Gao, Hengkang Wang. Feasibility assessment of up-flow anaerobic sludge blanket treatment of sulfamethoxazole pharmaceutical wastewater[J]. Front. Environ. Sci. Eng., 2018, 12(5): 13-.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed