Biodegradation

, Volume 29, Issue 2, pp 129–140 | Cite as

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

  • Fei Mao
  • Xiaohong Liu
  • Kang Wu
  • Chen Zhou
  • Youbin Si
Original Paper
First Online:
Received:
Accepted:

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.

Keywords

Antibiotic resistance Biodegradation Shewanella oneidensis MR-1 Shewanella sp. strain MR-4 Sulfonamides 
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Notes

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].

References

  1. 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 8:251–259CrossRefGoogle Scholar
  2. Ankley GT, Brooks BW, Huggett DB, Sumpter JP (2007) Repeating history: pharmaceuticals in the environment. Environ Sci Tech 41:8211–8217CrossRefGoogle Scholar
  3. 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 366:772–783CrossRefPubMedGoogle Scholar
  4. 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 53:696–702CrossRefPubMedGoogle Scholar
  5. 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 158:1444–1450CrossRefPubMedGoogle Scholar
  6. Eibes G, Debernardi G, Feijoo G, Moreira M, Lema J (2011) Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 22:539–550CrossRefPubMedGoogle Scholar
  7. Elcey CD, Kunhi AAM (2010) Substantially enhanced degradation of hexachlorocyclohexane isomers by a microbial consortium on acclimation. J Agric Food Chem 58:1046–1054CrossRefPubMedGoogle Scholar
  8. 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 278:193–199CrossRefPubMedGoogle Scholar
  9. 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 49:5505–5512Google Scholar
  10. Gauthier H, Yargeau V, Cooper DG (2010) Biodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism. Sci Total Environ 408:1701–1706CrossRefPubMedGoogle Scholar
  11. 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 4:1–8Google Scholar
  12. 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 73:492–498CrossRefGoogle Scholar
  13. 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 48:1670–1675CrossRefPubMedPubMedCentralGoogle Scholar
  14. Homem V, Santos L (2011) Degradation and removal methods of antibiotics from aqueous matrices. J Environ Manag 92:2304–2347CrossRefGoogle Scholar
  15. 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 98:4671–4681CrossRefGoogle Scholar
  16. 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 76:85–88CrossRefPubMedGoogle Scholar
  17. 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 407:4652–4664CrossRefPubMedGoogle Scholar
  18. 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 PubMedPubMedCentralGoogle Scholar
  19. 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 36:1202–1211CrossRefPubMedGoogle Scholar
  20. Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005a) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2086CrossRefPubMedGoogle Scholar
  21. Kumar K, Gupta SC, Chander Y, Singh AK (2005b) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54CrossRefGoogle Scholar
  22. Kümmerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75:417–434CrossRefPubMedGoogle Scholar
  23. Larcher S, Yargeau V (2011) Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biot 91:211–218CrossRefGoogle Scholar
  24. Larcher S, Yargeau V (2012) Biodegradation of sulfamethoxazole: current knowledge and perspectives. Appl Microbiol Biot 96:309–318CrossRefGoogle Scholar
  25. 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 282:158–164CrossRefPubMedGoogle Scholar
  26. Liu Y, Guan YT, Gao BY, Yue QY (2012) Antioxidant responses and degradation of two antibiotic contaminants in Microcystis aeruginosa. Ecotoxicol Environ Saf 86:23–30CrossRefPubMedGoogle Scholar
  27. 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):4793–4801CrossRefPubMedGoogle Scholar
  28. 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 92:969–978CrossRefPubMedGoogle Scholar
  29. 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 PubMedGoogle Scholar
  30. Nnenna FP, Lekiah P, Obemeata O (2011) Degradation of antibiotics by bacteria and fungi from the aquatic environment. J Toxicol Environ Health Sci 3:275–285Google Scholar
  31. 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 26:2172–2180CrossRefGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. Park H (2012) Reduction of antibiotics using microorganisms containing glutathione S-transferases under immobilized conditions. Environ Toxicol Pharmacol 34:345–350CrossRefPubMedGoogle Scholar
  34. 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 53:28–52CrossRefPubMedGoogle Scholar
  35. 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 405:377–384CrossRefGoogle Scholar
  36. 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 48:348–351CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 280:741–749CrossRefPubMedGoogle Scholar
  38. 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 79:5550–5558CrossRefPubMedPubMedCentralGoogle Scholar
  39. Rodayan A, Roy R, Yargeau V (2010) Oxidation products of sulfamethoxazole in ozonated secondary effluent. J Hazard Mater 177:237–243CrossRefPubMedGoogle Scholar
  40. 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 72:3236–3244CrossRefGoogle Scholar
  41. Sanz JL, RodrõÂguez N, Amils R (1996) The action of antibiotics on the anaerobic digestion process. Appl Microbiol Biotechnol 46:587–592CrossRefPubMedGoogle Scholar
  42. 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 108:8714–8719CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 34:2433–2441CrossRefPubMedGoogle Scholar
  44. 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 30:2839–2850CrossRefPubMedGoogle Scholar
  45. Suzuki S, Phuong HPT (2012) Ditribution of quinolones, sulfonamide, tetracyclines in aquqtic environment and antibiotic resistance in Indochina. Front Microbiol 3:67–68PubMedPubMedCentralGoogle Scholar
  46. 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 26:139–150CrossRefPubMedGoogle Scholar
  47. 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 42:173–178CrossRefPubMedGoogle Scholar
  48. 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 49:705–724CrossRefPubMedGoogle Scholar
  49. 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 670:111–123CrossRefGoogle Scholar
  50. Wang Q, Yates SR (2008) Laboratory study of oxytetracycline degradation kinetics in animal manure and soil. J Agric Food Chem 56:1683–1688CrossRefPubMedGoogle Scholar
  51. 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 88:322–328CrossRefPubMedGoogle Scholar
  52. 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 407:2711–2723CrossRefPubMedGoogle Scholar
  53. 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):e60460CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zarfl C, Matthies M, Klasmeier J (2008) A mechanistical model for the uptake of sulfonamides by bacteria. Chemosphere 70:753–760CrossRefPubMedGoogle Scholar
  55. Zhang YL, Marrs CF, Simon C, Xi CW (2009) Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci Total Environ 407:3702–3706CrossRefPubMedGoogle Scholar
  56. 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 28:447–452CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Fei Mao
    • 1
  • Xiaohong Liu
    • 1
  • Kang Wu
    • 1
  • Chen Zhou
    • 1
  • Youbin Si
    • 1
  1. 1.School of Resources and EnvironmentAnhui Agricultural UniversityHefeiChina

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