Insights on Sulfamethoxazole Bio-Transformation by Environmental Proteobacteria Isolates
Abstract
Although sulfonamide residues are frequently reported as freshwaters contaminants, information on the ability of native bacteria to modify these synthetic antibiotics is scarce. Our purpose was to investigate the potential of bacteria from different aquatic environments to cleave or transform sulfamethoxazole (SMX) and infer on their ability to reduce the toxicity of this antibiotic. From a collection of about 100 Proteobacteria, 47 strains previously isolated from drinking water, surface water, and wastewater grew in the presence of 200 μM SMX, and were further studied. Out of these, 14 strains, mostly from mineral drinking water, transformed SMX into equimolar amounts of the lesser toxic derivative N 4-acetyl-sulfamethoxazole. The highest percentage of SMX transformation was recorded for two strains affiliated to Pseudomonas mandelii. For P. mandelii McBPA4 higher SMX transformation rate and extent were observed in fed-batch (∼8 μM SMX/h, 81%) than in batch conditions (∼5 μM SMX/h, 25%), but similar specific transformation rates were found in both cultivation modes (∼20 μmol SMX/g cell dry weight/h), indicating the dependence of the process on the microbial load. These results evidence that the capacity to transform synthetic antibiotics may be common among bacteria and highlight the potential of environmental bacteria in attenuating the potential adverse effects of pollution with sulfonamides.
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Acetylsulfamethoxazole has reduced biological activity/toxicity compared to sulfamethoxazole.
“acetylsulfamethoxazole’s reduced biological activity/toxicity compared to sulfamethoxazole may limit the relevance of measuring it [12,42,43].”
From Pharmacometabolomics Study of Sulfamethoxazole and Trimethoprim in Kidney Transplant Recipients: Real-World Metabolism and Urinary Excretion (2025) · cites this paper as [43]
Cites
Hall, T. A. (1999) · Nucleic Acids Symposium Series · doi:10.14601/phytopathol_mediterr-14998u1.29 · Cited by 38,373 · see citing works
Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., & Buxton, H. T. (2002) · Environmental Science & Technology · doi:10.1021/es011055j · Cited by 7,953 · see citing works
Antibiotics in the aquatic environment – A review – Part I
Kümmerer, K. (2009) · Chemosphere · doi:10.1016/j.chemosphere.2008.11.086 · Cited by 4,485 · see citing works
Occurrence of Antibiotics in the Aquatic Environment
Hirsch, R., Ternes, T., Haberer, K., & Kratz, K.-L. (1999) · Science of The Total Environment · doi:10.1016/s0048-9697(98)00337-4 · Cited by 2,140 · see citing works
Pal, A., Gin, K. Y., Lin, A. Y., & Reinhard, M. (2010) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2010.09.026 · Cited by 1,169 · see citing works
Bacterial Degradation of Aromatic Compounds
Seo, J.-S., Keum, Y.-S., & Li, Q. X. (2009) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph6010278 · Cited by 968 · see citing works
Kümmerer, K. (2004) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkh325 · Cited by 940 · see citing works
Bacterial resistance to antibiotics: Enzymatic degradation and modification
WRIGHT, G. (2005) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2005.04.002 · Cited by 897 · see citing works
Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2003.tb01073.x · Cited by 889 · see citing works
Fatta-Kassinos, D., Meriç, S., & Nikolaou, A. (2011) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-010-4300-9 · Cited by 885 · see citing works
Molecular basis of bacterial resistance to chloramphenicol and florfenicol
Schwarz, Š., Kehrenberg, C., Doublet, B., & Cloeckaert, A. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.04.001 · Cited by 803 · see citing works
Fate of antibiotics during municipal water recycling treatment processes
Le-Minh, N., Khan, S. J., Drewes, J. E., & Stuetz, R. M. (2010) · Water Research · doi:10.1016/j.watres.2010.06.020 · Cited by 778 · see citing works
Göbel, A., Thomsen, A., McArdell, C. S., Joss, A., & Giger, W. (2005) · Environmental Science & Technology · doi:10.1021/es048550a · Cited by 760 · see citing works
Sulfonamide resistance: mechanisms and trends.
Sköld, O. (2000) · Drug Resistance Updates · doi:10.1054/drup.2000.0146 · Cited by 647 · see citing works
Sáenz, Y., Briñas, L., Domínguez, E., Ruiz, J., Zarazaga, M., Vilà, J., & Torres, C. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.10.3996-4001.2004 · Cited by 464 · see citing works
Trovó, A. G., Nogueira, R. F. P., Agüera, A., Sirtori, C., & Fernández‐Alba, A. R. (2009) · Chemosphere · doi:10.1016/j.chemosphere.2009.09.065 · Cited by 324 · see citing works
Schaider, L. A., Rudel, R. A., Ackerman, J. M., Dunagan, S. C., & Brody, J. G. (2014) · Science of The Total Environment · doi:10.1016/j.scitotenv.2013.08.067 · Cited by 304 · see citing works
Maynard, C., Fairbrother, J. M., Békal, S., et al. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.10.3214-3221.2003 · Cited by 300 · see citing works
Kassotaki, E., Buttiglieri, G., Ferrando‐Climent, L., Rodríguez‐Roda, I., & Pijuan, M. (2016) · Water Research · doi:10.1016/j.watres.2016.02.022 · Cited by 274 · see citing works
Yang, S., Lin, C., Lin, A. Y., et al. (2011) · Water Research · doi:10.1016/j.watres.2011.03.052 · Cited by 257 · see citing works
Ecotoxicity evaluation of selected sulfonamides
Białk‐Bielińska, A., Stolte, S., Arning, J., Uebers, U., Böschen, A., Stepnowski, P., & Matzke, M. (2011) · Chemosphere · doi:10.1016/j.chemosphere.2011.06.058 · Cited by 252 · see citing works
Fate of the Antibiotic Sulfamethoxazole and Its Two Major Human Metabolites in a Water Sediment Test
Radke, M., Lauwigi, C., Heinkele, G., Mürdter, T. E., & Letzel, M. (2009) · Environmental Science & Technology · doi:10.1021/es900300u · Cited by 230 · see citing works
Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1
Reis, P. J. M., Reis, A. C., Ricken, B., Kolvenbach, B. A., Manaia, C. M., Corvini, P. F.-X., & Nunes, O. C. (2014) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2014.08.039 · Cited by 221 · see citing works
Self-citationDiversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants
Figueira, V., Vaz‐Moreira, I., Silva, M., & Manaia, C. M. (2011) · Water Research · doi:10.1016/j.watres.2011.08.021 · Cited by 220 · see citing works
Self-citationBiodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism
Gauthier, H., Yargeau, V., & Cooper, D. G. (2010) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2009.12.012 · Cited by 218 · see citing works
Jiang, B., Li, A., Cui, D., Cai, R., Ma, F., & Wang, Y. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5488-3 · Cited by 218 · see citing works
Diversity and Antibiotic Resistance Patterns of Sphingomonadaceae Isolates from Drinking Water
Vaz‐Moreira, I., Nunes, O. C., & Manaia, C. M. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.00579-11 · Cited by 218 · see citing works
Self-citationWang, L., Liu, Y., Ma, J., et al. (2015) · Water Research · doi:10.1016/j.watres.2015.10.030 · Cited by 215 · see citing works
Sulfamethoxazole degradation in anaerobic sulfate-reducing bacteria sludge system
Jia, Y., Khanal, S. K., Zhang, H., Chen, G.-H., & Lu, H. (2017) · Water Research · doi:10.1016/j.watres.2017.04.040 · Cited by 213 · see citing works
Majewsky, M., Wagner, D., Delay, M., Bräse, S., Yargeau, V., & Horn, H. (2014) · Chemical Research in Toxicology · doi:10.1021/tx500267x · Cited by 194 · see citing works
Biodegradation of sulfamethoxazole in bacteria from three different origins
Mulla, S. I., Hu, A., Sun, Q., Li, J., Suanon, F., Ashfaq, M. A., & Yu, C. (2017) · Journal of Environmental Management · doi:10.1016/j.jenvman.2017.10.029 · Cited by 191 · see citing works
Xu, B., Mao, D., Luo, Y., & Xu, L. (2011) · Bioresource Technology · doi:10.1016/j.biortech.2011.04.086 · Cited by 178 · see citing works
Biodegradation of sulfamethoxazole by individual and mixed bacteria
Larcher, S., & Yargeau, V. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-011-3257-8 · Cited by 173 · see citing works
Topp, E., Chapman, R. A., Devers‐Lamrani, M., et al. (2012) · Journal of Environmental Quality · doi:10.2134/jeq2012.0162 · Cited by 166 · see citing works
Mohatt, J. L., Hu, L., Finneran, K. T., & Strathmann, T. J. (2011) · Environmental Science & Technology · doi:10.1021/es200413g · Cited by 160 · see citing works
Ricken, B., Corvini, P. F.-X., Cichocka, D., et al. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.00911-13 · Cited by 158 · see citing works
Aquatic Environmental Risk Assessment for Human Use of the Old Antibiotic Sulfamethoxazole in Europe
Straub, J. O. (2015) · Environmental Toxicology and Chemistry · doi:10.1002/etc.2945 · Cited by 154 · see citing works
Biodegradation of sulfamethoxazole: current knowledge and perspectives
Larcher, S., & Yargeau, V. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4326-3 · Cited by 145 · see citing works
Nödler, K., Licha, T., Barbieri, M., & Pérez, S. (2012) · Water Research · doi:10.1016/j.watres.2012.01.028 · Cited by 127 · see citing works
Bassin, I. D., Souza, B. S., Pereira, J. H. O. S., Moreira, F. C., Dezotti, M., Boaventura, R. A. R., & Vilar, V. J. P. (2014) · Chemical Engineering Journal · doi:10.1016/j.cej.2014.03.020 · Cited by 126 · see citing works
Self-citationBouju, H., Ricken, B., Beffa, T., et al. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05888-11 · Cited by 123 · see citing works
Biodegradation and metabolic pathway of sulfamethoxazole by a novel strain Acinetobacter sp.
Wang, S., & Wang, J. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8562-4 · Cited by 112 · see citing works
Sulfonamides in the environment: a review and a case report
Hruška, K., & Fránek, M. (2012) · Veterinární Medicína · doi:10.17221/4969-vetmed · Cited by 111 · see citing works
Bottled mineral water as a potential source of antibiotic resistant bacteria
Falcone-Dias, M. F., Vaz‐Moreira, I., & Manaia, C. M. (2012) · Water Research · doi:10.1016/j.watres.2012.04.007 · Cited by 104 · see citing works
Self-citationTappe, W., Herbst, M., Hofmann, D., et al. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03636-12 · Cited by 102 · see citing works
Redox-sensitivity and mobility of selected pharmaceutical compounds in a low flow column experiment
Banzhaf, S., Nödler, K., Licha, T., et al. (2012) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2012.08.041 · Cited by 94 · see citing works
Herzog, B., Lemmer, H., Horn, H., et al. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-276 · Cited by 85 · see citing works
Proteomic Analysis of 17β-Estradiol Degradation by Stenotrophomonas maltophilia
Li, Z., Nandakumar, R., Madayiputhiya, N., & Li, X. (2012) · Environmental Science & Technology · doi:10.1021/es300273k · Cited by 83 · see citing works
Diversity and antibiotic resistance of Acinetobacter spp. in water from the source to the tap
Narciso‐da‐Rocha, C., Vaz‐Moreira, I., Svensson‐Stadler, L., et al. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4190-1 · Cited by 82 · see citing works
Sulphonamide Residues in Italian Surface and Drinking Waters: A Small Scale Reconnaissance
Perret, D., Gentili, A., Marchese, S., Greco, A., & Curini, R. (2006) · Chromatographia · doi:10.1365/s10337-006-0737-6 · Cited by 80 · see citing works
Barreiros, L., Nogales, B., Manaia, C. M., et al. (2003) · Environmental Microbiology · doi:10.1046/j.1462-2920.2003.00492.x · Cited by 72 · see citing works
Self-citationZhang, Y.-B., Zhou, J., Xu, Q.-M., et al. (2016) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2016.05.063 · Cited by 72 · see citing works
Removal of sulfamethazine antibiotics by aerobic sludge and an isolated Achromobacter sp. S-3
Huang, M., Tian, S., Chen, D., et al. (2012) · Journal of Environmental Sciences · doi:10.1016/s1001-0742(11)60973-x · Cited by 69 · see citing works
Zhang, W., Wen, Y.-Y., Niu, Z., Yin, K., Xu, D., & Chen, L. (2011) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-011-0834-z · Cited by 63 · see citing works
Cribb, A. E., Nakamura, H., Grant, D. M., Miller, M. A., & Spielberg, S. P. (1993) · Biochemical Pharmacology · doi:10.1016/0006-2952(93)90280-a · Cited by 62 · see citing works
Assessment of copper and zinc salts as selectors of antibiotic resistance in Gram-negative bacteria
Becerra-Castro, C., Machado, R. A., Vaz‐Moreira, I., & Manaia, C. M. (2015) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2015.05.102 · Cited by 61 · see citing works
Self-citationNarciso‐da‐Rocha, C., & Manaia, C. M. (2016) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2016.04.062 · Cited by 58 · see citing works
Self-citationMajewsky, M., Glauner, T., & Horn, H. (2015) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-015-8748-5 · Cited by 57 · see citing works
Jung, C. M., Heinze, T. M., Strakosha, R., et al. (2009) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2008.04026.x · Cited by 50 · see citing works
Genotypic diversity and antibiotic resistance in Sphingomonadaceae isolated from hospital tap water
Narciso‐da‐Rocha, C., Vaz‐Moreira, I., & Manaia, C. M. (2013) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2013.06.109 · Cited by 47 · see citing works
Self-citationFigueira, V., Serra, E. A., Vaz‐Moreira, I., et al. (2011) · Journal of Water and Health · doi:10.2166/wh.2011.002 · Cited by 44 · see citing works
Pluvinage, B., Dairou, J., Possot, O. M., et al. (2007) · Biochemistry · doi:10.1021/bi700351w · Cited by 43 · see citing works
Isolation and characterization of Pseudomonas sp. DX7 capable of degrading sulfadoxine
Zhang, W., Xu, D., Niu, Z., et al. (2011) · Biodegradation · doi:10.1007/s10532-011-9522-9 · Cited by 37 · see citing works
Barreiros, L., Fernandes, A., Ferreira, A. C. S., et al. (2008) · Microbiology · doi:10.1099/mic.0.2007/015297-0 · Cited by 32 · see citing works
Acetylation and nitrosation of ciprofloxacin by environmental strains of mycobacteria
Adjei, M. D., Heinze, T. M., Deck, J., et al. (2007) · Canadian Journal of Microbiology · doi:10.1139/w06-101 · Cited by 30 · see citing works
Influence ofNAT2Polymorphisms on Sulfamethoxazole Pharmacokinetics in Renal Transplant Recipients
Kagaya, H., Miura, M., Niioka, T., Saito, M., Numakura, K., Habuchi, T., & Satoh, S. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.05037-11 · Cited by 23 · see citing works
Aminoglycosides: Mechanisms of Action and Resistance
Magalhães, M. D. L. B., & Blanchard, J. S. (2009) · Humana Press eBooks · doi:10.1007/978-1-59745-180-2_14 · Cited by 18 · see citing works
Kim, D., Feng, J., Chen, H., et al. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.02347-12 · Cited by 18 · see citing works
Souza, B. M., Marinho, B., Moreira, F. C., Dezotti, M., Boaventura, R., & Vilar, V. (2017) · Environmental science and pollution research international · doi:10.1007/s11356-015-5690-1 · Cited by 16 · see citing works
Self-citationComplete Genome Sequence of Achromobacter denitrificans PR1
Reis, A. C., Kroll, K., Gomila, M., et al. (2017) · Genome Announcements · doi:10.1128/genomea.00762-17 · Cited by 12 · see citing works
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Hof, M. A. J., de Haan, H., Stepanovic, S., Bakker, S. J. L., Hak, E., Hopfgartner, G., Klont, F., & Investigators, T. (2025) · Metabolites · doi:10.3390/metabo15070473 · Cited by 1 · see citing works
“Admittedly, acetylsulfamethoxazole’s reduced biological activity/toxicity compared to sulfamethoxazole may limit the relevance of measuring it [12,42,43].”
- Authors
- Reis, P. J. M., Homem, V., Alves, A., Vilar, V. J. P., Manaia, C. M., & Nunes, O. C.
- Affiliations
- Universidade do Porto (PT)
- Universidade Católica Portuguesa (PT)
- Corresponding author
- Nunes, Olga C.
- Venue
- Journal of Hazardous Materials
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 358
- Pages
- 310-318
- ISSN
- 0304-3894 (ISSN-L)
- OpenAlex
- W2810136725
- Cited by
- 80
- References
- 70
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 9 · 2023: 6 · 2022: 14 · 2021: 16 · 2020: 6 · 2019: 8 · 2018: 1 · 2016: 1
- FWCI
- 2.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Hazardous Materials (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion)
- Funders
- European Regional Development Fund (ERDF)
- FCT - Fundação para a Ciência e a Tecnologia
- North Portugal Regional Operational Programme
- QREN-POPH
- Topics
- Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
- Physical Sciences › Environmental Science › Environmental Chemistry › Environmental Chemistry and Analysis
- Physical Sciences › Environmental Science › Pollution › Pesticide and Herbicide Environmental Studies
- Keywords
- sulfamethoxazole, Proteobacteria, Pseudomonas mandelii, antibiotic degradation, wastewater bacteria, microbial load
- MeSH terms
- Biotransformation, Fresh Water, Genes, Bacterial, Kinetics, Models, Theoretical, Sulfamethoxazole, Water Pollutants, Chemical, Proteobacteria, Drinking Water, Wastewater
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