Anaerobic biodegradation of trimethoprim with sulfate as an electron acceptor

Bin Liang, Deyong Kong, Mengyuan Qi, Hui Yun, Zhiling Li, Ke Shi, E Chen, Alisa S. Vangnai, Aijie Wang

PDF(1379 KB)
PDF(1379 KB)
Front. Environ. Sci. Eng. ›› 2019, Vol. 13 ›› Issue (6) : 84. DOI: 10.1007/s11783-019-1168-6
RESEARCH ARTICLE
RESEARCH ARTICLE

Anaerobic biodegradation of trimethoprim with sulfate as an electron acceptor

Author information +
History +

Highlights

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.

Abstract

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.

Graphical abstract

Keywords

Trimethoprim (TMP) biodegradation / Demethylation / Sulfate reduction / Core microbiome / Antibiotic fate

Cite this article

Download citation ▾
Bin Liang, Deyong Kong, Mengyuan Qi, Hui Yun, Zhiling Li, Ke Shi, E Chen, Alisa S. Vangnai, Aijie Wang. Anaerobic biodegradation of trimethoprim with sulfate as an electron acceptor. Front. Environ. Sci. Eng., 2019, 13(6): 84 https://doi.org/10.1007/s11783-019-1168-6

References

[1]
Allen T D, Kraus P F, Lawson P A, Drake G R, Balkwill D L, Tanner R S (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
CrossRef Pubmed Google scholar
[2]
Bache R, Pfennig N (1981). Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Archives of Microbiology, 130(3): 255–261
CrossRef Google scholar
[3]
Batt A L, Kim S, Aga D S (2006). Enhanced biodegradation of iopromide and trimethoprim in nitrifying activated sludge. Environmental Science & Technology, 40(23): 7367–7373
CrossRef Pubmed Google scholar
[4]
Benner J, De Smet D, Ho A, Kerckhof F M, Vanhaecke L, Heylen K, Boon N (2015). Exploring methane-oxidizing communities for the co-metabolic degradation of organic micropollutants. Applied Microbiology and Biotechnology, 99(8): 3609–3618
CrossRef Pubmed Google scholar
[5]
Bouju H, Ricken B, Beffa T, Corvini P F X, Kolvenbach B A (2012). Isolation of bacterial strains capable of sulfamethoxazole mineralization from an acclimated membrane bioreactor. Applied and Environmental Microbiology, 78(1): 277–279
CrossRef Pubmed Google scholar
[6]
Cetecioglu Z, Ince B, Orhon D, Ince O (2016). Anaerobic sulfamethoxazole degradation is driven by homoacetogenesis coupled with hydrogenotrophic methanogenesis. Water Research, 90: 79–89
CrossRef Pubmed Google scholar
[7]
Chen F, Li Z L, Yang J Q, Liang B, Lin X Q, Nan J, Wang A J (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
CrossRef Google scholar
[8]
Crofts T S, Wang B, Spivak A, Gianoulis T A, Forsberg K J, Gibson M K, Johnsky L A, Broomall S M, Rosenzweig C N, Skowronski E W, Gibbons H S, Sommer M O A, Dantas G (2018). Shared strategies for β-lactam catabolism in the soil microbiome. Nature Chemical Biology, 14(6): 556–564
Pubmed
[9]
Daghio M, Vaiopoulou E, Patil S A, Suárez-Suárez A, Head I M, Franzetti A, Rabaey K (2016). Anodes stimulate anaerobic toluene degradation via sulfur cycling in marine sediments. Applied and Environmental Microbiology, 82(1): 297–307
CrossRef Pubmed Google scholar
[10]
Deng Y, Li B, Zhang T (2018a). Bacteria that make a meal of sulfonamide antibiotics: Blind spots and emerging opportunities. Environmental Science & Technology, 52(7): 3854–3868
CrossRef Pubmed Google scholar
[11]
Deng Y, Mao Y, Li B, Yang C, Zhang T (2016). Aerobic degradation of sulfadiazine by Arthrobacter spp.: Kinetics, pathways, and genomic characterization. Environmental Science & Technology, 50(17): 9566–9575
CrossRef Pubmed Google scholar
[12]
Deng Y, Wang Y, Mao Y, Zhang T (2018b). Partnership of Arthrobacter and Pimelobacter in aerobic degradation of sulfadiazine revealed by metagenomics analysis and isolation. Environmental Science & Technology, 52(5): 2963–2972
CrossRef Pubmed Google scholar
[13]
Grabowski A, Tindall B J, Bardin V, Blanchet D, Jeanthon C (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
CrossRef Pubmed Google scholar
[14]
Haider M R, Jiang W L, Han J L, Sharif H M A, Ding Y C, Cheng H Y, Wang A J (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
CrossRef Google scholar
[15]
Han X, Scott A C, Fedorak P M, Bataineh M, Martin J W (2008). Influence of molecular structure on the biodegradability of naphthenic acids. Environmental Science & Technology, 42(4): 1290–1295
CrossRef Pubmed Google scholar
[16]
Huang L, Wang Q, Quan X, Liu Y, Chen G (2013). Bioanodes/biocathodes formed at optimal potentials enhance subsequent pentachlorophenol degradation and power generation from microbial fuel cells. Bioelectrochemistry (Amsterdam, Netherlands), 94: 13–22
CrossRef Pubmed Google scholar
[17]
Jewell K S, Castronovo S, Wick A, Falås P, Joss A, Ternes T A (2016). New insights into the transformation of trimethoprim during biological wastewater treatment. Water Research, 88: 550–557
CrossRef Pubmed Google scholar
[18]
Jia Y, Khanal S K, Shu H, Zhang H, Chen G H, Lu H (2018). Ciprofloxacin degradation in anaerobic sulfate-reducing bacteria (SRB) sludge system: Mechanism and pathways. Water Research, 136: 64–74
CrossRef Pubmed Google scholar
[19]
Jia Y, Khanal S K, Zhang H, Chen G H, Lu H (2017). Sulfamethoxazole degradation in anaerobic sulfate-reducing bacteria sludge system. Water Research, 119: 12–20
CrossRef Pubmed Google scholar
[20]
Jia Y, Zhang H, Khanal S K, Yin L, Lu H (2019). Insights into pharmaceuticals removal in an anaerobic sulfate-reducing bacteria sludge system. Water Research, 161: 191–201
CrossRef Pubmed Google scholar
[21]
Jiang B, Li A, Cui D, Cai R, Ma F, Wang Y (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
CrossRef Pubmed Google scholar
[22]
Jiang W L, Xia X, Han J L, Ding Y C, Haider M R, Wang A J (2018). Graphene modified electro-fenton catalytic membrane for in situ degradation of antibiotic florfenicol. Environmental Science & Technology, 52(17): 9972–9982
CrossRef Pubmed Google scholar
[23]
Kassotaki E, Buttiglieri G, Ferrando-Climent L, Rodriguez-Roda I, Pijuan M (2016). Enhanced sulfamethoxazole degradation through ammonia oxidizing bacteria co-metabolism and fate of transformation products. Water Research, 94: 111–119
CrossRef Pubmed Google scholar
[24]
Kleemann R, Meckenstock R U (2011). Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiology Ecology, 78(3): 488–496
CrossRef Pubmed Google scholar
[25]
Kong D, Liang B, Yun H, Cheng H, Ma J, Cui M, Wang A, Ren N (2015). Cathodic degradation of antibiotics: characterization and pathway analysis. Water Research, 72: 281–292
CrossRef Pubmed Google scholar
[26]
Li D, Qi R, Yang M, Zhang Y, Yu T (2011). Bacterial community characteristics under long-term antibiotic selection pressures. Water Research, 45(18): 6063–6073
CrossRef Pubmed Google scholar
[27]
Liang B, Cheng H, Van Nostrand J D, Ma J, Yu H, Kong D, Liu W, Ren N, Wu L, Wang A, Lee D J, Zhou J (2014). Microbial community structure and function of nitrobenzene reduction biocathode in response to carbon source switchover. Water Research, 54: 137–148
CrossRef Pubmed Google scholar
[28]
Liang B, Cheng H Y, Kong D Y, Gao S H, Sun F, Cui D, Kong F Y, Zhou A J, Liu W Z, Ren N Q, Wu W M, Wang A J, Lee D J (2013). Accelerated reduction of chlorinated nitroaromatic antibiotic chloramphenicol by biocathode. Environmental Science & Technology, 47(10): 5353–5361
CrossRef Pubmed Google scholar
[29]
Liang B, Ma J, Cai W, Li Z, Liu W, Qi M, Zhao Y, Ma X, Deng Y, Wang A, Zhou J (2019). Response of chloramphenicol-reducing biocathode resistome to continuous electrical stimulation. Water Research, 148: 398–406
CrossRef Pubmed Google scholar
[30]
Liu Q, Li M, Liu X, Zhang Q, Liu R, Wang Z, Shi X, Quan J, Shen X, Zhang F (2018). Removal of sulfamethoxazole and trimethoprim from reclaimed water and the biodegradation mechanism. Frontiers of Environmental Science & Engineering, 12(6): 6
[31]
Luo Y, Guo W, Ngo H H, Nghiem L D, Hai F I, Zhang J, Liang S, Wang X C C (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
CrossRef Pubmed Google scholar
[32]
Ma X, Qi M, Li Z, Zhao Y, Yan P, Liang B, Wang A (2019). Characterization of an efficient chloramphenicol-mineralizing bacterial consortium. Chemosphere, 222: 149–155
Pubmed
[33]
Pan L J, Tang X D, Li C X, Yu G W, Wang Y (2017). Biodegradation of sulfamethazine by an isolated thermophile-Geobacillus sp. S-07. World Journal of Microbiology & Biotechnology, 33(5): 85
CrossRef Pubmed Google scholar
[34]
Qiu L Q, Zhang L, Tang K, Chen G, Kumar Khanal S, Lu H (2019). Removal of sulfamethoxazole (SMX) in sulfate-reducing flocculent and granular sludge systems. Bioresource Technology, 288: 121592
CrossRef Pubmed Google scholar
[35]
Rasool K, Woo S H, Lee D S (2013). Simultaneous removal of COD and Direct Red 80 in a mixed anaerobic sulfate-reducing bacteria culture. Chemical Engineering Journal, 223: 611–616
CrossRef Google scholar
[36]
Reichenbecher W, Schink B (1997). Desulfovibrio inopinatus, sp. nov., a new sulfate-reducing bacterium that degrades hydroxyhydroquinone (1,2,4-trihydroxybenzene). Archives of Microbiology, 168(4): 338–344
CrossRef Pubmed Google scholar
[37]
Song X, Liu R, Chen L, Kawagishi T (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]
Sun L, Toyonaga M, Ohashi A, Tourlousse D M, Matsuura N, Meng X Y, Tamaki H, Hanada S, Cruz R, Yamaguchi T, Sekiguchi Y (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
CrossRef Pubmed Google scholar
[39]
Van Boeckel T P, Brower C, Gilbert M, Grenfell B T, Levin S A, Robinson T P, Teillant A, Laxminarayan R (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
CrossRef Pubmed Google scholar
[40]
van der Zaan B M, Saia F T, Stams A J, Plugge C M, de Vos W M, Smidt H, Langenhoff A A, Gerritse J (2012). Anaerobic benzene degradation under denitrifying conditions: Peptococcaceae as dominant benzene degraders and evidence for a syntrophic process. Environmental Microbiology, 14(5): 1171–1181
CrossRef Pubmed Google scholar
[41]
Wang L, Liu Y, Ma J, Zhao F (2016). Rapid degradation of sulphamethoxazole and the further transformation of 3-amino-5-methylisoxazole in a microbial fuel cell. Water Research, 88: 322–328
CrossRef Pubmed Google scholar
[42]
Wu H, Sun Q, Sun Y, Zhou Y, Wang J, Hou C, Jiang X, Liu X, Shen J (2019). Co-metabolic enhancement of 1H-1,2,4-triazole biodegradation through nitrification. Bioresource Technology, 271: 236–243
CrossRef Pubmed Google scholar
[43]
Xu X, Zarecki R, Medina S, Ofaim S, Liu X, Chen C, Hu S, Brom D, Gat D, Porob S, Eizenberg H, Ronen Z, Jiang J, Freilich S (2019). Modeling microbial communities from atrazine contaminated soils promotes the development of biostimulation solutions. The ISME Journal, 13(2): 494–508
CrossRef Pubmed Google scholar
[44]
Yang L, Yi G, Hou Y, Cheng H, Luo X, Pavlostathis S G, Luo S, Wang A (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
CrossRef Pubmed Google scholar
[45]
Yuan Y, Chen C, Liang B, Huang C, Zhao Y, Xu X, Tan W, Zhou X, Gao S, Sun D, Lee D, Zhou J, Wang A (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
CrossRef Pubmed Google scholar
[46]
Yun H, Kong D, Liang B, Cui M, Li Z, Wang A (2016). Response of anodic bacterial community to the polarity inversion for chloramphenicol reduction. Bioresource Technology, 221: 666–670
CrossRef Pubmed Google scholar
[47]
Yun H, Liang B, Qiu J, Zhang L, Zhao Y, Jiang J, Wang A (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
CrossRef Pubmed Google scholar
[48]
Zellner G, Kneifel H, Winter J (1990). Oxidation of benzaldehydes to benzoic acid derivatives by three Desulfovibrio strains. Applied and Environmental Microbiology, 56(7): 2228–2233
Pubmed
[49]
Zhang H, Khanal S K, Jia Y, Song S, Lu H (2019). Fundamental insights into ciprofloxacin adsorption by sulfate-reducing bacteria sludge: Mechanisms and thermodynamics. Chemical Engineering Journal, 378: 122103
CrossRef Google scholar
[50]
Zhang Q Q, Ying G G, Pan C G, Liu Y S, Zhao J L (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
CrossRef Pubmed Google scholar
[51]
Zhao Y, Bai Y, Guo Q, Li Z, Qi M, Ma X, Wang H, Kong D, Wang A, Liang B (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
CrossRef Pubmed Google scholar
[52]
Zhao Y, Li Z, Ma J, Yun H, Qi M, Ma X, Wang H, Wang A, Liang B (2018). Enhanced bioelectroremediation of a complexly contaminated river sediment through stimulating electroactive degraders with methanol supply. Journal of Hazardous Materials, 349: 168–176
CrossRef Pubmed Google scholar
[53]
Zhou J, He Q, Hemme C L, Mukhopadhyay A, Hillesland K, Zhou A, He Z, Van Nostrand J D, Hazen T C, Stahl D A, Wall J D, Arkin A P (2011). How sulphate-reducing microorganisms cope with stress: Lessons from systems biology. Nature Reviews. Microbiology, 9(6): 452–466
CrossRef Pubmed Google scholar

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 51808537), the China Postdoctoral Science Foundation (No. 2019M650866) the Key Research Program of the Chinese Academy of Sciences (No. KFZD-SW-219), the Youth Technology Fund Project of Gansu Province (No. 18JR3RA023), the Provincial Science and Technology Plan Projects of Gansu Province (No. 2015017) and the Youth Science and Technology Foundation of Gansu Province (No. 1506RJYA154).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-019-1168-6 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2019 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature
AI Summary AI Mindmap
PDF(1379 KB)

Accesses

Citations

Detail

Sections
Recommended

/