Skip to main content

Advertisement

Log in

Biodegradation of sulfonamides by Shewanella oneidensis MR-1 and Shewanella sp. strain MR-4

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

Because of extensive sulfonamides application in aquaculture and animal husbandry and the consequent increase in sulfonamides discharged into the environment, strategies to remediate sulfonamide-contaminated environments are essential. In this study, the resistance of Shewanella oneidensis MR-1 and Shewanella sp. strain MR-4 to the sulfonamides sulfapyridine (SPY) and sulfamethoxazole (SMX) were determined, and sulfonamides degradation by these strains was assessed. Shewanella oneidensis MR-1 and Shewanella sp. strain MR-4 were resistant to SPY and SMX concentrations as high as 60 mg/L. After incubation for 5 days, 23.91 ± 1.80 and 23.43 ± 2.98% of SPY and 59.88 ± 1.23 and 63.89 ± 3.09% of SMX contained in the medium were degraded by S. oneidensis MR-1 and Shewanella sp. strain MR-4, respectively. The effects of the initial concentration of the sulfonamides and initial pH of the medium on biodegradation, and the degradation of different sulfonamides were assessed. The products were measured by LC–MS; with SPY as a substrate, 2-AP (2-aminopyridine) was the main stable metabolite, and with SMX as a substrate, 3A5MI (3-amino-5-methyl-isoxazole) was the main stable metabolite. The co-occurrence of 2-AP or 3A5MI and 4-aminobenzenesulfonic acid suggests that the initial step in the biodegradation of the two sulfonamides is S–N bond cleavage. These results suggest that S. oneidensis MR-1 and Shewanella sp. strain MR-4 are potential bacterial resources for biodegrading sulfonamides and therefore bioremediation of sulfonamide-polluted environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Micro 8:251–259

    Article  CAS  Google Scholar 

  • Ankley GT, Brooks BW, Huggett DB, Sumpter JP (2007) Repeating history: pharmaceuticals in the environment. Environ Sci Tech 41:8211–8217

    Article  CAS  Google Scholar 

  • Brown KD, Kulis J, Thomson B, Chapman TH, Mawhinney DB (2006) Occurrence of antibiotics in hospital, residential, and dairy, effluent, municipal wastewater, and the Rio Grande in New Mexico. Sci Total Environ 366:772–783

    Article  CAS  PubMed  Google Scholar 

  • Byrne-Bailey KG, Gaze WH, Kay P, Boxall ABA, Hawkey PM, Wellington EMH (2009) Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom. Antimicrob Agents Chemother 53:696–702

    Article  CAS  PubMed  Google Scholar 

  • Chang X, Meyer MT, Liu XY, Zhao Q, Chen H, Chen JA, Qiu ZQ, Yang L, Cao J, Shu WQ (2010) Determination of antibiotics in sewage from hospitals, nursery and slaughter house, wastewater treatment plant and source water in Chongqing region of three Gorge Reservoir in China. Environ Pollut 158:1444–1450

    Article  CAS  PubMed  Google Scholar 

  • Eibes G, Debernardi G, Feijoo G, Moreira M, Lema J (2011) Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 22:539–550

    Article  CAS  PubMed  Google Scholar 

  • Elcey CD, Kunhi AAM (2010) Substantially enhanced degradation of hexachlorocyclohexane isomers by a microbial consortium on acclimation. J Agric Food Chem 58:1046–1054

    Article  CAS  PubMed  Google Scholar 

  • Enne VI, Cassar C, Sprigings K (2008) A high prevalence of antimicrobial resistant Escherchia coli isolated from pigs and a low prevalence of antimicrobial resistant E. coli from cattle and sheep in Great Britain at slaughter. FEMS Microbiol Lett 278:193–199

    Article  CAS  PubMed  Google Scholar 

  • García-Galán MJ, Rodríguez-Rodríguez CE, Vicent T, Caminal G, Díaz-Cruz MS, Barceló D (2012) Biodegradation of sulfamethazine by Trametes versicolor: removal from sewage sludge and identification of intermediate products by UPLC–QqTOF-MS. Sci Total Environ 49:5505–5512

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Glenn LM, Rl Lindsey, Folster JP (2013) Antimicrobial resistance genes in multidrug-resistant Salmonella enteria isolated from animals, retail meats and human in the United States and Canada. Microb Drug Resist 4:1–8

    Google Scholar 

  • Groh JL, Luo QW, Ballard JD, Krumholz LR (2007) Genes that enhance the ecological fitness of Shewanella oneidensis MR-1 in sediments reveal the value of antibiotic resistance. Appl Environ Microb 73:492–498

    Article  CAS  Google Scholar 

  • Héritier C, Poirel L, Nordmann P (2004) Genetic and biochemical characterization of a chromosome-encoded carbapenem-hydrolyzing ambler class D beta-lactamase from Shewanella algae. Antimicrob Agents Chemother 48:1670–1675

    Article  PubMed  PubMed Central  Google Scholar 

  • Homem V, Santos L (2011) Degradation and removal methods of antibiotics from aqueous matrices. J Environ Manag 92:2304–2347

    Article  CAS  Google Scholar 

  • Jiang BC, Li A, Cui D, Cai R, Ma F, Wang YN (2014) Biodegradation and metabolic pathway of sulfamethoxazole by Pseudomonas psychrophila HA-4, a newly isolated cold-adapted sulfamethoxazole-degrading bacterium. Appl Microbiol Biot 98:4671–4681

    Article  CAS  Google Scholar 

  • Kang CH, Shin YJ, Jeon HE, Choi JH, Jeong SY, So JS (2013) Antibiotic resistance of Shewanella putrefaciens isolated from shellfish collected from the West Sea in Korea. Mar Pollut Bull 76:85–88

    Article  CAS  PubMed  Google Scholar 

  • Karci A, Balcioglu IA (2009) Investigation of the tetracycline, sulfonamide, and fluoroquinolone antimicrobial compounds in animal manure and agricultural soils in Turkey. Sci Total Environ 407:4652–4664

    Article  CAS  PubMed  Google Scholar 

  • Karpinets TV, Romine MF, Schmoyer DD, Kora GH, Syed MH, Leuze MR, Serres MH, Park BH, Samatova NF, Uberbacher EC (2010) Shewanella knowledgebase: integration of the experimental data and computational predictions suggests a biological role for transcription of intergenic regions. Database. https://doi.org/10.1093/database/baq012

    PubMed  PubMed Central  Google Scholar 

  • Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005a) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2086

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Gupta SC, Chander Y, Singh AK (2005b) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54

    Article  CAS  Google Scholar 

  • Kümmerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75:417–434

    Article  PubMed  Google Scholar 

  • Larcher S, Yargeau V (2011) Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biot 91:211–218

    Article  CAS  Google Scholar 

  • Larcher S, Yargeau V (2012) Biodegradation of sulfamethoxazole: current knowledge and perspectives. Appl Microbiol Biot 96:309–318

    Article  CAS  Google Scholar 

  • Lin B, Lyu J, Lyu XJ, Yu HQ, Zhong H, Lam JCW (2014) Characterization of cefalexin degradation capabilities of two Pseudomonas strains isolated from activated sludge. J Hazard Mater 282:158–164

    Article  PubMed  Google Scholar 

  • Liu Y, Guan YT, Gao BY, Yue QY (2012) Antioxidant responses and degradation of two antibiotic contaminants in Microcystis aeruginosa. Ecotoxicol Environ Saf 86:23–30

    Article  CAS  PubMed  Google Scholar 

  • 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(11):4793–4801

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1007/s10532-017-9789-6

    PubMed  Google Scholar 

  • Nnenna FP, Lekiah P, Obemeata O (2011) Degradation of antibiotics by bacteria and fungi from the aquatic environment. J Toxicol Environ Health Sci 3:275–285

    CAS  Google Scholar 

  • Nödler K, Licha T, Fischer S, Wagner B, Sauter M (2011) A case study on the correlation of micro-contaminants and potassium in the Leine River (Germany). Appl Geochem 26:2172–2180

    Article  Google Scholar 

  • Pan LJ, Tang XD, Li CX, Yu GW, Wang Y (2017) Biodegradation of sulfamethazine by an isolated thermophile–Geobacillus sp. S-07. World J Microbiol Biotechnol 33:85. https://doi.org/10.1007/s11274-017-2245-2

    Article  PubMed  Google Scholar 

  • Park H (2012) Reduction of antibiotics using microorganisms containing glutathione S-transferases under immobilized conditions. Environ Toxicol Pharmacol 34:345–350

    Article  CAS  PubMed  Google Scholar 

  • Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, Nightingale C, Preston R, Waddell J (2004) Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother 53:28–52

    Article  CAS  PubMed  Google Scholar 

  • Phuong HPT, Nonaka L, Hung VP (2008) Detection of the sul1, sul2 and sul3 genes in sulfonamide-resistant bacteria from wastewater and shrimp ponds of North Vietnam. Sci Total Environ 405:377–384

    Article  Google Scholar 

  • Poirel L, Héritier C, Nordmann P (2004) Chromosome-encoded ambler class D beta-lactamase of Shewanella oneidensis as a progenitor of carbapenem-hydrolyzing oxacillinase. Antimicrob Agents Chemother 48:348–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodayan A, Roy R, Yargeau V (2010) Oxidation products of sulfamethoxazole in ozonated secondary effluent. J Hazard Mater 177:237–243

    Article  CAS  PubMed  Google Scholar 

  • Roh Y, Gao HC, Vali H, Kennedy DW, Yang ZK, Gao WM, Dohnalkova AC, Stapleton RD, Moon JW, Phelps TJ, Fredrickson JK, Zhou JZ (2006) Metal reduction and iron biomineralization by a Psychrotolerant Fe(III)-reducing bacterium, Shewanella sp. strain PV-4. Appl Environ Microb 72:3236–3244

    Article  CAS  Google Scholar 

  • Sanz JL, RodrõÂguez N, Amils R (1996) The action of antibiotics on the anaerobic digestion process. Appl Microbiol Biotechnol 46:587–592

    Article  CAS  PubMed  Google Scholar 

  • Schaefer JK, Rocks SS, Zheng W, Liang LY, Gu BH, Morel FMM (2011) Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc Natl Acad Sci USA 108:8714–8719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selvam A, Zhao Z, Li Y, Chen Y, Leung KS, Wong JW (2013) Degradation of tetracycline and sulfadiazine during continuous thermophilic composting of pig manure and sawdust. Environ Technol 34:2433–2441

    Article  CAS  PubMed  Google Scholar 

  • Selvi A, Salam JA, Das N (2014) Biodegradation of cefdinir by a novel yeast strain, Ustilago sp. SMN03 isolated from pharmaceutical wastewater. World J Microbiol Biotechnol 30:2839–2850

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Phuong HPT (2012) Ditribution of quinolones, sulfonamide, tetracyclines in aquqtic environment and antibiotic resistance in Indochina. Front Microbiol 3:67–68

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Topp E, Chapman R, Devers-Lamrani M, Hartmann A, Marti R, Martin-Laurent F, Sabourin L, Scott A, Sumarah M (2013) 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

    Article  CAS  PubMed  Google Scholar 

  • Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49:705–724

    Article  CAS  PubMed  Google Scholar 

  • Vree TB, Schoondermarkvande Ven E, Verweyvan Wissen CP, Bars AM, Swolfs A, Van Galen PM, Amatdjais Groenen H (1995) Isolation, identification and determination of sulfadiazine and its hydroxy metabolites and conjugates from man and rhesus monkey by high-performance liquid chromatography. J Chromatogr B 670:111–123

    Article  CAS  Google Scholar 

  • Wang Q, Yates SR (2008) Laboratory study of oxytetracycline degradation kinetics in animal manure and soil. J Agric Food Chem 56:1683–1688

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Liu YL, 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

    Article  CAS  PubMed  Google Scholar 

  • Watkinson AJ, Murby EJ, Kolpin DW, Costanzo SD (2009) The occurrence of antibiotics in an urban watershed: from wastewater to drinking water. Sci Total Environ 407:2711–2723

    Article  CAS  PubMed  Google Scholar 

  • Yin JH, Sun LL, Dong YY, Chi X, Zhu WM, Qi SH, Gao HC (2013) Expression of blaA underlies unexpected ampicillin-Induced cell lysis of Shewanella oneidensis. PLoS ONE 8(3):e60460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarfl C, Matthies M, Klasmeier J (2008) A mechanistical model for the uptake of sulfonamides by bacteria. Chemosphere 70:753–760

    Article  CAS  PubMed  Google Scholar 

  • Zhang YL, Marrs CF, Simon C, Xi CW (2009) Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci Total Environ 407:3702–3706

    Article  CAS  PubMed  Google Scholar 

  • Zhang WW, Wen YY, Niu ZL, Yin K, Xu DX, Chen LX (2012) Isolation and characterization of sulfonamide-degrading bacteria Escherichia sp. HS21 and Acinetobacter sp. HS51. World J Microb Biot 28:447–452

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China [Grant Number 41471405], and the Project of Agricultural Public Welfare Scientific Research [Grant Number 201303101-06].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Youbin Si.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mao, F., Liu, X., Wu, K. et al. Biodegradation of sulfonamides by Shewanella oneidensis MR-1 and Shewanella sp. strain MR-4. Biodegradation 29, 129–140 (2018). https://doi.org/10.1007/s10532-017-9818-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-017-9818-5

Keywords

Navigation