Abstract
Sulfonamides are the oldest class of synthetic antibiotics still in use in clinical and veterinary settings. The intensive utilization of sulfonamides has been leading to the widespread contamination of the environment with these xenobiotic compounds. Consequently, in addition to pathogens and commensals, also bacteria inhabiting a wide diversity of environmental compartments have been in contact with sulfonamides for almost 90 years. This review aims at giving an overview of the effect of sulfonamides on bacterial cells, including the strategies used by bacteria to cope with these bacteriostatic agents. These include mechanisms of antibiotic resistance, co-metabolic transformation, and partial or total mineralization of sulfonamides. Possible implications of these mechanisms on the ecosystems and dissemination of antibiotic resistance are also discussed.
Key points
• Sulfonamides are widespread xenobiotic pollutants;
• Target alteration is the main sulfonamide resistance mechanism observed in bacteria;
• Sulfonamides can be modified, degraded, or used as nutrients by some bacteria.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Achermann S, Bianco V, Mansfeldt CB, Vogler B, Kolvenbach BA, Corvini PFX, Kathrin Fenner K (2018) Biotransformation of sulfonamide antibiotics in activated sludge: the formation of pterin-conjugates leads to sustained risk. Environ Sci Technol 52(11):6265–6274. https://doi.org/10.1021/acs.est.7b06716
Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, Huynh W, Nguyen A-LV, Cheng AA, Liu S, Min SY, Miroshnichenko A, Tran H-K, Werfalli RE, Nasir JA, Oloni M, Speicher DJ, Florescu A, Singh B, Faltyn M, Hernandez-Koutoucheva A, Sharma AN, Bordeleau E, Pawlowski AC, Zubyk HL, Dooley D, Griffiths E, Maguire F, Winsor GL, Beiko RG, Brinkman FSL, Hsiao WWL, Domselaar GV, McArthur AG (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48(D1):D517–D525. https://doi.org/10.1093/nar/gkz935
Alvarino T, Nastold P, Suarez S, Omil F, Corvini PFX, Bouju H (2016) Role of biotransformation, sorption and mineralization of 14C-labelled sulfamethoxazole under different redox conditions. Sci Total Environ 542:706–715. https://doi.org/10.1016/j.scitotenv.2015.10.140
Banzhaf S, Nödler K, Licha T, Krein A, Scheytt T (2012) Redox-sensitivity and mobility of selected pharmaceutical compounds in a low flow column experiment. Sci Total Environ 438:113–121. https://doi.org/10.1016/j.scitotenv.2012.08.041
Baptiste KE, Kyvsgaard NC (2017) Do antimicrobial mass medications work? A systematic review and meta-analysis of randomised clinical trials investigating antimicrobial prophylaxis or metaphylaxis against naturally occurring bovine respiratory disease. Pathog Dis 75(7):ftx083. https://doi.org/10.1093/femspd/ftx083
Baran W, Adamek E, Ziemiańska J, Sobczak A (2011) Effects of the presence of sulfonamides in the environment and their influence on human health. J Hazard Mater 196:1–15. https://doi.org/10.1016/j.jhazmat.2011.08.082
Barbieri M, Carrera J, Ayora C, Sanchez-Vila X, Licha T, Nödler K, Osorio V, Pérez S, Köck-Schulmeyer M, López de Alda M, Barceló D (2012) Formation of diclofenac and sulfamethoxazole reversible transformation products in aquifer material under denitrifying conditions: batch experiments. Sci Total Environ 426:256–263. https://doi.org/10.1016/j.scitotenv.2012.02.058
Barreiros L, Fernandes A, Silva Ferreira AC, Pereira H, Bastos MMSM, Manaia CM, Nunes OC (2008) New insights into a bacterial metabolic and detoxifying association responsible for the mineralization of the thiocarbamate herbicide molinate. Microbiol-SGM 154(4):1038–1046. https://doi.org/10.1099/mic.0.2007/015297-0
Blair JMA, Richmond GE, Piddock LJV (2014) Multidrug efflux pumps in Gram-negative bacteria and their role in antibiotic resistance. Future Microbiol 9:10–1177. https://doi.org/10.2217/fmb.14.66
Bouju H, Ricken B, Beffa T, Corvini PFX, Kolvenbach BA (2012) Isolation of bacterial strains capable of sulfamethoxazole mineralization from an acclimated membrane bioreactor. Appl Environ Microbiol 78:277–279. https://doi.org/10.1128/AEM.05888-11
Buffet-Bataillon S, Le Jeune A, Le Gall-David S, Bonnaure-Mallet M, Jolivet-Gougeon A (2012) Molecular mechanisms of higher MICs of antibiotics and quaternary ammonium compounds for Escherichia coli isolated from bacteraemia. J Antimicrob Chemother 67(12):2837–2842. https://doi.org/10.1093/jac/dks321
Cao L, Zhang J, Zhao R, Deng Y, Liu J, Fu W, Lei Y, Zhang T, Li X, Li B (2019) Genomic characterization, kinetics, and pathways of sulfamethazine biodegradation by Paenarthrobacter sp. A01. Environ Int 131:104961. https://doi.org/10.1016/j.envint.2019.104961
Chang B-V, Chang Y-T, Chao W-L, Yeh S-L, Kuo D-L, Yang C-W (2019) Effects of sulfamethoxazole and sulfamethoxazole-degrading bacteria on water quality and microbial communities in milkfish ponds. Environ Pollut 252:305–316. https://doi.org/10.1016/j.envpol.2019.05.136
Charuaud L, Jarde E, Jaffrezic A, Thomas M-F, Le Bot B (2019) Veterinary pharmaceutical residues from natural water to tap water: sales, occurrence and fate. J Hazard Mater 361:169–186. https://doi.org/10.1016/j.jhazmat.2018.08.075
Chen J, Xie S (2018) Overview of sulfonamide biodegradation and the relevant pathways and microorganisms. Sci Total Environ 640–641:1465–1477. https://doi.org/10.1016/j.scitotenv.2018.06.016
Chen J, Jiang X, Tong T, Miao S, Huang J, Xie S (2019) Sulfadiazine degradation in soils: dynamics, functional gene, antibiotic resistance genes and microbial community. Sci Total Environ 691:1072–1081. https://doi.org/10.1016/j.scitotenv.2019.07.230
Cheng S, Shi M, Xing L, Wang X, Gao H, Sun Y (2020) Sulfamethoxazole affects the microbial composition and antibiotic resistance gene abundance in soil and accumulates in lettuce. Environ Sci Pollut Res 27:29257–29265. https://doi.org/10.1007/s11356-020-08902-1
Coenen S, Adriaenssens N, Versporten A, Muller A, Minalu G, Faes C, Vankerckhoven V, Aerts M, Hens N, Molenberghs G, Goossens H, ESAC Project Group (2011) European surveillance of antimicrobial consumption (ESAC): outpatient use of tetracyclines, sulphonamides and trimethoprim, and other antibacterials in Europe (1997–2009). J Antimicrob Chemother 66:vi57–vi70. https://doi.org/10.1093/jac/dkr458
Collins SL, Patterson AD (2020) The gut microbiome: an orchestrator of xenobiotic metabolism. Acta Pharm Sin B 10(1):19–32. https://doi.org/10.1016/j.apsb.2019.12.001
Connor EE (1998) Sulfonamide antibiotics. Prim Care Update Ob Gyns 5(1):32–35. https://doi.org/10.1016/S1068-607X(97)00121-2
Cribb AE, Spielberg SP (1992) Sulfamethoxazole is metabolized to the hydroxylamine in humans. Clin Pharmacol Ther 51:522–526. https://doi.org/10.1038/clpt.1992.57
Cribb AE, Nakamura H, Grant DM, Miller MA, Spielberg SP (1993) Role of polymorphic and monomorphic human arylamine N-acetyltransferases in determining sulfamethoxazole metabolism. Biochem Pharmacol 45:1277–1282. https://doi.org/10.1016/0006-2952(93)90280-A
Cycoń M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Front Microbiol 10:338. https://doi.org/10.3389/fmicb.2019.00338
Deng Y, Mao Y, Li B, Yang C, Zhang T (2016) Aerobic degradation of sulfadiazine by Arthrobacter spp.: kinetics, pathways, and genomic characterization. Environ Sci Technol 50:9566–9575. https://doi.org/10.1021/acs.est.6b02231
Deng Y, Li B, Zhang T (2018) Bacteria that make a meal of sulfonamide antibiotics: blind spots and emerging opportunities. Environ Sci Technol 52(7):3854–3868. https://doi.org/10.1021/acs.est.7b06026
Ding G-C, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014) Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One 9(3):e92958. https://doi.org/10.1371/journal.pone.0092958
Felis E, Kalka J, Sochacki A, Kowalska K, Bajkacz S, Harnisz M, Korzeniewska E (2020) Antimicrobial pharmaceuticals in the aquatic environment - occurrence and environmental implications. Eur J Pharmacol 866:172813. https://doi.org/10.1016/j.ejphar.2019.172813
Fenu A, Donckels BMR, Beffa T, Bemfohr C, Weemaes M (2015) Evaluating the application of Microbacterium sp. strain BR1 for the removal of sulfamethoxazole in full-scale membrane bioreactors. Water Sci Technol 72:1754–1761. https://doi.org/10.2166/wst.2015.397
García-Galán MJ, Díaz-Cruz MS, Barceló D (2008) Identification and determination of metabolites and degradation products of sulfonamide antibiotics. Trends Anal Chem 27:1008–1022. https://doi.org/10.1016/j.trac.2008.10.001
Gauthier H, Yargeau V, Cooper DG (2010) Biodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism. Sci Total Environ 408:1701–1706. https://doi.org/10.1016/j.scitotenv.2009.12.012
Gaynes R (2017) The discovery of penicillin-new insights after more than 75 years of clinical use. Emerg Infect Dis 23(5):849–853. https://doi.org/10.3201/eid2305.161556
Gelband H, Miller-Petrie M, Pant S, Gandra S, Levinson J, Barter D, White A, Laxminarayan R (2015) State of the world’s antibiotics. Center for Disease Dynamics, Economics & Policy. CDDEP: Washington, D.C
Geng C, Zhuang Y, Bergheaud V, Garnier P, Haudin C-S (2019) Fate of 14C-acetyl sulfamethoxazole during the activated sludge process. Environ Sci Pollut Res 26:9832–9841. https://doi.org/10.1007/s11356-019-04360-6
Hendriksen RS, Munk P, Njage P, van Bunnik B, McNally L, Lukjancenko O, Röder T, Nieuwenhuijse D, Pedersen SK, Kjeldgaard J, Kaas RS, Clausen PTLC, Vogt JK, Leekitcharoenphon P, van de Schans MGM, Zuidema T, Husman AMR, Rasmussen S, Petersen B, Global Sewage Surveillance project consortium, Amid C, Cochrane G, Sicheritz-Ponten T, Schmitt H, JRM A, Aidara-Kane A, Pamp SJ, Lund O, Hald T, Woolhouse M, Koopmans MP, Vigre H, Petersen TN, Aarestrup FM (2019) Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nat Commun 10:1124. https://doi.org/10.1038/s41467-019-08853-3
Hu S, Hu H, Li W, Hong X, Cai D, Lin J, Li M, Zhao Y (2020) Investigating the biodegradation of sulfadiazine in soil using Enterobacter cloacae T2 immobilized on bagasse. RSC Adv 10(2):1142–1151. https://doi.org/10.1039/C9RA07302G
Huovinen P, Sundström L, Swedberg G, Sköld O (1995) Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 39:279–289. https://doi.org/10.1128/aac.39.2.279
Islas-Espinoza M, Reid BJ, Wexler M, Bond PL (2012) Soil bacterial consortia and previous exposure enhance the biodegradation of sulfonamides from pig manure. Microb Ecol 64:140–151. https://doi.org/10.1007/s00248-012-0010-5
Jia Y, Kumar Khanal SK, Zhang H, Chen G-H, Lu H (2017) Sulfamethoxazole degradation in anaerobic sulfate-reducing bacteria sludge system. Water Res 119:12–20. https://doi.org/10.1016/j.watres.2017.04.040
Jia Y, Zhang H, Khanal SK, Yin L, Lu H (2019) Insights into pharmaceuticals removal in an anaerobic sulfate-reducing bacteria sludge system. Water Res 161:191–201. https://doi.org/10.1016/j.watres.2019.06.010
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. Appl Microbiol Biotechnol 98:4671–4681. https://doi.org/10.1007/s00253-013-5488-3
Kagaya H, Miura M, Niioka T, Saito M, Numakura K, Habuchi T, Satoh S (2012) Influence of NAT2 polymorphisms on sulfamethoxazole pharmacokinetics in renal transplant recipients. Antimicrob Agents Chemother 56:825–829. https://doi.org/10.1128/AAC.05037-11
Kassotaki E, Buttiglieri G, Ferrando-Climent L, Rodriguez-Roda I, Pijuana M (2016) Enhanced sulfamethoxazole degradation through ammonia oxidizing bacteria co-metabolism and fate of transformation products. Water Res 94:111–119. https://doi.org/10.1016//j.watres.2016.02.022
Kim D-W, Cung CN, Lee K, Wellington EMH, Cha C-J (2019) A novel sulfonamide resistance mechanism by two-component flavin-dependent monooxygenase system in sulfonamide-degrading actinobacteria. Environ Int 127:206–215. https://doi.org/10.1016/j.envint.2019.03.046
Koba O, Golovko O, Kodešová R, Fér M, Grabic R (2017) Antibiotics degradation in soil: a case of clindamycin, trimethoprim, sulfamethoxazole and their transformation products. Environ Pollut 220:1251–1263. https://doi.org/10.1016/j.envpol.2016.11.007
Kugel S, Baunach M, Baer P, Ishida-Ito M, Sundaram S, Xu Z, Groll M, Hertweck C (2017) Cryptic indole hydroxylation by a non-canonical terpenoid cyclase parallels bacterial xenobiotic detoxification. Nat Commun 8:15804. https://doi.org/10.1038/ncomms15804
Larcher S, Yargeau V (2011) Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biotechnol 91:211–218. https://doi.org/10.1007/s00253-011-3257-8
Li X, Yu H, Xu S, Hua R (2013) Uptake of three sulfonamides from contaminated soil by pakchoi cabbage. Ecotoxicol Environ Saf 92:297–302. https://doi.org/10.1016/j.ecoenv.2013.03.010
Liao X, Li B, Zou R, Xie S, Yuan B (2016) Antibiotic sulfanilamide biodegradation by acclimated microbial populations. Appl Microbiol Biotechnol 100:2439–2447. https://doi.org/10.1007/s00253-015-7133-9
Liu S, Zhao H, Lehmler H-J, Cai X, Chen J (2017) Antibiotic pollution in marine food webs in Laizhou Bay, North China: trophodynamics and human exposure implication. Environ Sci Technol 51(4):2392–2400. https://doi.org/10.1021/acs.est.6b04556
Lubroth J, Ormel HJ, Otto P, Patriarchi A, Wall BA, Mateus A, Marshall L, Pfeiffer DU (2016) Drivers, dynamics and epidemiology of antimicrobial resistance in animal production. FAO. ISBN: 978-92-5-109441-9
Majewsky M, Wagner D, Delay M, Bräse S, Yargeau V, Horn H (2014) Antibacterial activity of sulfamethoxazole transformation products (TPs): general relevance for sulfonamide TPs modified at the para position. Chem Res Toxicol 27:1821–1828. https://doi.org/10.1021/tx500267x
Man Y, Wang J, Tam NF-Y, Wan X, Huang W, Zheng Y, Tang J, Tao R, Yang Y (2020) Responses of rhizosphere and bulk substrate microbiome to wastewater-borne sulfonamides in constructed wetlands with different plant species. Sci Total Environ 706:135955. https://doi.org/10.1016/j.scitotenv.2019.135955
Mao F, Liu X, Wu K, Zhou C, Si Y (2018) Biodegradation of sulfonamides by Shewanella oneidensis MR-1 and Shewanella sp. strain MR-4. Biodegradation 29(2):129–140. https://doi.org/10.1007/s10532-017-9818-5
Martínez-Carballo E, González-Barreiro C, Scharf S, Gans O (2007) Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environ Pollut 148(2):570–579. https://doi.org/10.1016/j.envpol.2006.11.035
Mohatt JL, Hu L, Finneran KT, Strathmann TJ (2011) Microbially mediated abiotic transformation of the antimicrobial agent sulfamethoxazole under iron-reducing soil conditions. Environ Sci Technol 45:4793–4801. https://doi.org/10.1021/es200413g
Mohring SAI, Strzysch I, Fernandes MR, Kiffmeyer TK, Tuerk J, Hamscher G (2009) Degradation and elimination of various sulfonamides during anaerobic fermentation: a promising step on the way to sustainable pharmacy? Environ Sci Technol 43:2569–2574. https://doi.org/10.1021/es802042d
Muaz K, Riaz M, Akhtar S, Park S, Ismail A (2018) Antibiotic residues in chicken meat: global prevalence, threats, and decontamination strategies: a review. J Food Prot 81(4):619–627. https://doi.org/10.4315/0362-028X.JFP-17-086
Mulla SI, Sun Q, Hu A, Wang Y, Ashfaq M, Eqani SAMAS, Yu C-P (2016) Evaluation of sulfadiazine degradation in three newly isolated pure bacterial cultures. PLoSOne 11(10):e0165013. https://doi.org/10.1371/journal.pone.0165013
Mulla SI, Hu A, Sun Q, Li J, Suanona F, Ashfaq M, Yu C-P (2018) Biodegradation of sulfamethoxazole in bacteria from three different origins. J Environ Manag 206:93–102. https://doi.org/10.1016/j.jenvman.2017.10.029
Müller E, Schüssler W, Horn H, Lemmer H (2013) Aerobic biodegradation of the sulfonamide antibiotic sulfamethoxazole by activated sludge applied as co-substrate and sole carbon and nitrogen source. Chemosphere 92:969–978. https://doi.org/10.1016/j.chemosphere.2013.02.070
Munk P, Knudsen BE, Lukjancenko O, Duarte ASR, Van Gompel L, Luiken REC, Smit LAM, Schmitt H, Garcia AD, Hansen RB, Petersen TN, Bossers A, Ruppé E, EFFORT Group, Lund O, Hald T, Pamp SJ, Vigre H, Heederik D, Wagenaar JA, Mevius D, Aarestrup FM (2018) Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 3:898–908. https://doi.org/10.1038/s41564-018-0192-9
Na G, Fang X, Cai Y, Ge L, Zong H, Yuan X, Yao Z, Zhang Z (2013) Occurrence, distribution, and bioaccumulation of antibiotics in coastal environment of Dalian, China. Mar Pollut Bull 69(1–2):233–237. https://doi.org/10.1016/j.marpolbul.2012.12.028
Narciso-da-Rocha C, Rocha J, Vaz-Moreira I, Lira F, Tamames J, Henriques I, Martinez JL, Manaia CM (2018) Bacterial lineages putatively associated with the dissemination of antibiotic resistance genes in a full-scale urban wastewater treatment plant. Environ Int 118:179–188. https://doi.org/10.1016/j.envint.2018.05.040
Nguyen PY, Carvalho G, Reis AC, Nunes OC, Reis MAM, Oehmen A (2017) Impact of biogenic substrates on sulfamethoxazole biodegradation kinetics by Achromobacter denitrificans strain PR1. Biodegradation 28:1–13. https://doi.org/10.1007/s10532-017-9789-6
Nguyen PY, Silva AF, Reis AC, Nunes OC, Rodrigues AM, Rodrigues JE, Cardoso VV, Benoliel MJ, Reis MAM, Oehmen A, Carvalho G (2019) Bioaugmentation of membrane bioreactor with Achromobacter denitrificans strain PR1 for enhanced sulfamethoxazole removal in wastewater. Sci Total Environ 648:44–55. https://doi.org/10.1016/j.scitotenv.2018.08.100
Nödler K, Licha T, Barbieri M, Pérez S (2012) Evidence for the microbially mediated abiotic formation of reversible and non-reversible sulfamethoxazole transformation products during denitrification. Water Res 46:2131–2139. https://doi.org/10.1016/j.watres.2012.01.028
Ouyang W-Y, Su J-Q, Richnow HH, Lorenz Adrian L (2019) Identification of dominant sulfamethoxazole-degraders in pig farm-impacted soil by DNA and protein stable isotope probing. Environ Int 126:118–126. https://doi.org/10.1016/j.envint.2019.02.001
Pärnänen KMM, Narciso-da-Rocha C, Kneis D, Berendonk TU, Cacace D, Do TT, Elpers C, Fatta-Kassinos D, Henriques I, Jaeger T, Karkman A, Martinez JL, Michael SG, Michael-Kordatou I, O’Sullivan K, Rodriguez-Mozaz S, Schwartz T, Sheng H, Sørum H, Stedtfeld RD, Tiedje JM, Giustina SVD, Walsh F, Vaz-Moreira I, Virta M, Manaia CM (2019) Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence. Sci Adv 5(3):eaau9124. https://doi.org/10.1126/sciadv.aau9124
Partridge SR, Kwong SM, Firth N, Jensen SO (2018) Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 31(4):e00088–e00017. https://doi.org/10.1128/CMR.00088-17
Perri R, Kolvenbach BA, Corvini PFX (2020) Subsistence and complexity of antimicrobial resistance on a community-wide level. Environ Microbiol 22:2463–2468. https://doi.org/10.1111/1462-2920.15018
Pluvinage B, Dairou J, Possot OM, Martins M, Fouet A, Rodrigues-Lima F (2007) Cloning and molecular characterization of three arylamine N-acetyltransferase genes from Bacillus anthracis: identification of unusual enzymatic properties and their contribution to sulfamethoxazole resistance. Biochemistry 46:7069–7078. https://doi.org/10.1021/bi700351w
Pormohammad A, Nasiri MJ, Azimi T (2019) Prevalence of antibiotic resistance in Escherichia coli strains simultaneously isolated from humans, animals, food, and the environment: a systematic review and meta-analysis. Infect Drug Resist 12:1181–1197. https://doi.org/10.2147/IDR.S201324
Qvarnstrom Y, Swedberg G (2006) Variations in gene organization and DNA uptake signal sequence in the folP region between commensal and pathogenic Neisseria species. BMC Microbiol 6:11. https://doi.org/10.1186/1471-2180-6-11
Radke M, Lauwigi C, Heinkele G, Múrdter TE, Letzel M (2009) Fate of the antibiotic sulfamethoxazole and its two major human metabolites in a water sediment test. Environ Sci Technol 43:3135–3141. https://doi.org/10.1021/es900300u
Rang HP, Dale MM, Ritter JM, Moore PK (2003) Pharmacology, 5th edn. Churchill Livingstone, Edinburgh
Razavi M, Marathe NP, Gillings MR, Flach C-F, Kristiansson E, Joakim Larsson DG (2017) Discovery of the fourth mobile sulfonamide resistance gene. Microbiome 5:160–172. https://doi.org/10.1186/s40168-017-0379-y
Reis AC, Nunes OC (2020) Personal communication
Reis PJM, Reis AC, Ricken B, Kolvenbach BA, Manaia CM, Corvini PFX, Nunes OC (2014) Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1. J Hazard Mater 280:741–749. https://doi.org/10.1016/j.jhazmat.2014.08.039
Reis PJM, Homem V, Alves A, Vilar VJP, Manaia CM, Nunes OC (2018a) Insights on sulfamethoxazole bio-transformation by environmental Proteobacteria isolates. J Hazard Mater 358:310–318. https://doi.org/10.1016/j.jhazmat.2018.07.012
Reis AC, Čvančarová M, Liu Y, Lenz M, Hettich T, Kolvenbach BA, Corvini PF-X, Nunes OC (2018b) Biodegradation of sulfamethoxazole by a bacterial consortium of Achromobacter denitrificans PR1 and Leucobacter sp. GP. Appl Microbiol Biotechnol 102:10299–10314. https://doi.org/10.1007/s00253-018-9411-9
Reis AC, Kolvenbach BA, Chami M, Gales L, Egas C, Corvini PF-X, Nunes OC (2019) Comparative genomics reveals a novel genetic organization of the sad cluster in the sulfonamide-degrader ‘Candidatus Leucobacter sulfamidivorax’ strain GP. BMC Genomics 20:885. https://doi.org/10.1186/s12864-019-6206-z
Reis AC, Kolvenbach BA, Nunes OC, Corvini PFX (2020a) Biodegradation of antibiotics: the new resistance determinants – part II. New Biotechnol 54:13–27. https://doi.org/10.1016/j.nbt.2019.08.003
Reis AC, Kolvenbach BA, Nunes OC, Corvini PFX (2020b) Biodegradation of antibiotics: the new resistance determinants – part I. New Biotechnol 54:34–51. https://doi.org/10.1016/j.nbt.2019.08.002
Revuelta JL, Serrano-Amatriain C, Ledesma-Amaro R, Jiménez A (2018) Formation of folates by microorganisms: towards the biotechnological production of this vitamin. Appl Microbiol Biotechnol 102(20):8613–8620. https://doi.org/10.1007/s00253-018-9266-0
Ricken B, Corvini PFX, Cichocka D, Parisi M, Lenz M, Wyss D, Martínez-Lavanchy PM, Müller JA, Shahgaldian P, Tulli LG, Kohler H-PE, Kolvenbach BA (2013) Ipso-hydroxylation and subsequent fragmentation: a novel microbial strategy to eliminate sulfonamide antibiotics. Appl Environ Microbiol 79:5550–5558. https://doi.org/10.1128/aem.00911-13
Ricken B, Fellmann O, Kohler H-PE, Schäffer A, Corvini PF-X, Kolvenbach BA (2015) Degradation of sulfonamide antibiotics by Microbacterium sp. strain BR1 – elucidating the downstream pathway. New Biotechnol 32:710–715. https://doi.org/10.1016/j.nbt.2015.03.005
Ricken B, Kolvenbach BA, Bergesch C, Benndorf D, Kroll K, Strnad H, Vlček Č, Adaixo R, Hammes F, Shahgaldian P, Schäffer A, Kohler H-PE, Corvini PF-X (2017) FMNH2-dependent monooxygenases initiate catabolism of sulfonamides in Microbacterium sp. strain BR1 subsisting on sulfonamide antibiotics. Sci Rep 7:15783. https://doi.org/10.1038/s41598-017-16132-8
Rogowska J, Cieszynska-Semenowicz M, Ratajczyk W, Wolska L (2020) Micropollutants in treated wastewater. Ambio 49:487–503. https://doi.org/10.1007/s13280-019-01219-5
Saccá ML, Barra Caracciolo A, Di Lenola M, Grenni P (2017) Ecosystem services provided by soil microorganisms. In: Lukac M, Grenni P, Gamboni M (eds) Soil biological communities and ecosystem resilience. Sustainability in pant and crop protection. Springer, Cham, pp 9–24. https://doi.org/10.1007/978-3-319-63336-7_2
Sánchez MB, Martínez JL (2015) The efflux pump SmeDEF contributes to trimethoprim-sulfamethoxazole resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 59(7):4347–4348. https://doi.org/10.1128/AAC.00714-15
Sánchez-Osuna M, Cortés P, Barbé J, Erill I (2019) Origin of the mobile di-hydro-pteroate synthase gene determining sulfonamide resistance in clinical isolates. Front Microbiol 9:3332. https://doi.org/10.3389/fmicb.2018.03332
Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759. https://doi.org/10.1016/j.chemosphere.2006.03.026
Shambaugh GE (1966) History of sulfonamides. Arch Otolaryngol 83(1):1–2. https://doi.org/10.1001/archotol.1966.00760020003001
Sköld O (2000) Sulfonamide resistance: mechanisms and trends. Drug Resist Updat 3:155–160. https://doi.org/10.1054/drup.2000.0146
Sneader S (2007) Sulfonamides (the history). In: Van Nostrand’s Scientific Encyclopedia. Wiley, Inc. https://doi.org/10.1002/9780471743989.vse10173
Song M, Luo C, Jiang L, Peng K, Zhang D, Zhang R, Li Y, Zhang G (2019) The presence of in situ sulphamethoxazole degraders and their interactions with other microbes in activated sludge as revealed by DNA stable isotope probing and molecular ecological network analysis. Environ Int 124:121–129. https://doi.org/10.1016/j.envint.2018.12.039
Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964. https://doi.org/10.1038/35023079
Tappe W, Herbst M, Hofmann D, Koeppchen S, Kummer S, Thiele B, Groeneweg J (2013) Degradation of sulfadiazine by Microbacterium lacus strain SDZm4, isolated from lysimeters previously manured with slurry from sulfadiazine-medicated pigs. Appl Environ Microbiol 79:2572–2577. https://doi.org/10.1128/aem.03636-12
Tappe W, Hofmann D, Disko U, Koeppchen S, Kummer S, Vereecken H (2015) A novel isolated Terrabacter-like bacterium can mineralize 2-aminopyrimidine, the principal metabolite of microbial sulfadiazine degradation. Biodegradation 26:139–150. https://doi.org/10.1007/s10532-015-9722-9
Topp E, Chapman R, Devers-Lamrani M, Hartmann A, Marti R, Martin-Laurent F, Sabourin L, Scott A, Sumarah M (2012) Accelerated biodegradation of veterinary antibiotics in agricultural soil following long-term exposure, and isolation of a sulfamethazine-degrading Microbacterium sp. J Environ Qual 42:173–178. https://doi.org/10.2134/jeq2012.0162
Urra J, Alkorta I, Garbisu C (2019) Potential benefits and risks for soil health derived from the use of organic amendments in agriculture. Agronomy 9:542. https://doi.org/10.3390/agronomy9090542
Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41:241–267. https://doi.org/10.1080/10409230600817422
Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014) Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14:742–750. https://doi.org/10.1016/s1473-3099(14)70780-7
Varsha YM, Naga Deepthi CH, Chenna S (2011) An emphasis on xenobiotic degradation in environmental cleanup. J Bioremed Biodegrad S11:001. https://doi.org/10.4172/2155-6199.S11-001
Vree TB, Hekster YA (1985) Renal excretion of sulfonamides. Antibiot Chemother:66–120. https://doi.org/10.1159/000410273
Wall DH, Nielsen UN (2012) Biodiversity and ecosystem services: is it the same below ground? Nat Educ Knowl 3(12):8. https://www.nature.com/scitable/knowledge/library/biodiversity-and-ecosystem-services-is-it-the-96677163/. Accessed Sept 2020
Wang S, Wang J (2018a) Biodegradation and metabolic pathway of sulfamethoxazole by a novel strain Acinetobacter sp. Appl Microbiol Biotechnol 102:425–432. https://doi.org/10.1007/s00253-017-8562-4
Wang J, Wang S (2018b) Microbial degradation of sulfamethoxazole in the environment. Appl Microbiol Biotechnol 102:3573–3582. https://doi.org/10.1007/s00253-018-8845-4
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 Res 88:322–328. https://doi.org/10.1016/j.watres.2015.10.030
Wang S, Hu Y, Wang J (2018a) Biodegradation of typical pharmaceutical compounds by a novel strain Acinetobacter sp. J Environ Manag 217:240–246. https://doi.org/10.1016/j.jenvman.2018.03.096
Wang L, You L, Zhang J, Yang T, Zhang W, Zhang Z, Liu P, Wu S, Zhao F, Ma J (2018b) Biodegradation of sulfadiazine in microbial fuel cells: reaction mechanism, biotoxicity removal and the correlation with reactor microbes. J Hazard Mater 360:402–411. https://doi.org/10.1016/j.jhazmat.2018.08.021
Wei C-H, Sanchez-Huerta C, Leiknes T, Amy G, Zhou H, Hu X, Fang Q, Rong H (2019) Removal and biotransformation pathway of antibiotic sulfamethoxazole from municipal wastewater treatment by anaerobic membrane bioreactor. J Hazard Mater 380:120894. https://doi.org/10.1016/j.jhazmat.2019.120894
Xiong W, Sun Y, Ding X, Wang M, Zeng Z (2015) Selective pressure of antibiotics on ARGs and bacterial communities in manure-polluted freshwater-sediment microcosms. Front Microbiol 6:194. https://doi.org/10.3389/fmicb.2015.00194
Xu B, Mao D, Luo Y, Xu L (2011) Sulfamethoxazole biodegradation and biotransformation in the water-sediment system of a natural river. Bioresour Technol 102:7069–7076. https://doi.org/10.1016/j.biortech.2011.04.086
Xue W, Li F, Zhou Q (2019) Degradation mechanisms of sulfamethoxazole and its induction of bacterial community changes and antibiotic resistance genes in a microbial fuel cell. Bioresour Technol 289:121632. https://doi.org/10.1016/j.biortech.2019.121632
Yang N, Wan J, Zhao S, Wang Y (2015) Removal of concentrated sulfamethazine by acclimatized aerobic sludge and possible metabolic products. PeerJ 3:e1359. https://doi.org/10.7717/peerj.1359
Yang C, Song G, Lim W (2020) A review of the toxicity in fish exposed to antibiotics. Comp Biochem Physiol C Toxicol Pharmacol 237:108840. https://doi.org/10.1016/j.cbpc.2020.108840
Yousef F, Mansour O, Herbali J (2018) Sulfonamides: historical discovery development (structure-activity relationship notes). In-vitro In-vivo In-silico Journal 1(1):1–15. https://doi.org/10.2174/138955713804484749
Yu L, Wang Y, Su X, Fu Y, Ma F, Guo H (2020) Biodiversity, isolation and genome analysis of sulfamethazine-degrading bacteria using high-throughput analysis. Bioprocess Biosyst Eng 43:1521–1531. https://doi.org/10.1007/s00449-020-02345-1
Zhang Y-B, Zhou J, Xu Q-M, Cheng J-S, Luo Y-L, Yuan Y-J (2016) Exogenous cofactors for the improvement of bioremoval and biotransformation of sulfamethoxazole by Alcaligenes faecalis. Sci Total Environ 565:547–556. https://doi.org/10.1016/j.scitotenv.2016.05.063
Zhang S, Song H-L, Cao X, Li H, Guo J, Yang X-L, Singh RP, Liu S (2019) Inhibition of methanogens decreased sulfadiazine removal and increased antibiotic resistance gene development in microbial fuel cells. Bioresour Technol 281:188–194. https://doi.org/10.1016/j.biortech.2019.02.089
Zheng J, Wang S, Zhou A, Zhao B, Dong J, Zhao X, Li P, Yue X (2020) Efficient elimination of sulfadiazine in an anaerobic denitrifying circumstance: biodegradation characteristics, biotoxicity removal and microbial community analysis. Chemosphere 252:126472. https://doi.org/10.1016/j.chemosphere.2020.126472
Zhou L-J, Han P, Yu Y, Wang B, Men Y, Wagner M, Wu QL (2019) Cometabolic biotransformation and microbial-mediated abiotic transformation of sulfonamides by three ammonia oxidizers. Water Res 159:444–453. https://doi.org/10.1016/j.watres.2019.05.031
Acknowledgments
We thank Patrícia J.M. Reis, Ana C. Reis, and Ana Rita L. Ribeiro for their support in the elaboration of this work.
Funding
This work was supported by Base Funding-UIDB/00511/2020 of the Laboratory for Process Engineering, Environment, Biotechnology and Energy (LEPABE) funded by national funds through Fundação para a Ciência e a Tecnologia (FCT)/MCTES (PIDDAC), and FCT project UID/Multi/50016/2019 (Associate Laboratory CBQF). We also received support from the European Union’s Horizon 2020 research and innovation program under grant agreement 826244.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
All the authors participated in the elaboration of this work.
Consent for publication
All the authors consent to the publication of this work.
Code availability
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 199 kb)
Rights and permissions
About this article
Cite this article
Nunes, O.C., Manaia, C.M., Kolvenbach, B.A. et al. Living with sulfonamides: a diverse range of mechanisms observed in bacteria. Appl Microbiol Biotechnol 104, 10389–10408 (2020). https://doi.org/10.1007/s00253-020-10982-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10982-5