Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 10069–10079 | Cite as

Fungi extracellular enzyme-containing microcapsules enhance degradation of sulfonamide antibiotics in mangrove sediments

Research Article

Abstract

Mangroves represent a special coastal vegetation along the coastlines of tropical and subtropical regions. Sulfonamide antibiotics (SAs) are the most commonly used antibiotics. The application of white-rot fungi extracellular enzyme-containing microcapsules (MC) for aerobic degradation of SAs in mangrove sediments was investigated in this study. Degradation of three SAs, sulfamethoxazole (SMX), sulfadimethoxine (SDM), and sulfamethazine (SMZ), was enhanced by adding MC to the sediments. The order of SA degradation in batch experiments was SMX > SDM > SMZ. Bioreactor experiments revealed that SA removal rates were higher with than without MC. The enhanced SA removal rates with MC persisted with three re-additions of SAs. Thirteen bacteria genera (Achromobacter, Acinetobacter, Alcaligenes, Aquamicrobium, Arthrobacter, Brevundimonas, Flavobacterium, Methylobacterium, Microbacterium, Oligotropha, Paracoccus, Pseudomonas, and Rhodococcus) were identified to be associated with SA degradation in mangrove sediments by combination of next-generation sequencing, bacterial strain isolation, and literature search results. Results of this study suggest that MC could be used for SA removal in mangrove sediments.

Keywords

Sulfonamide antibiotics Degradation Mangrove sediment Microbial community Microcapsules 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Andrade LL, Leite DC, Ferreira EM, Ferreira LQ, Paula GR, Maguire MJ, Hubert CR, Peixoto RS, Domingues RM, Rosado AS (2012) Microbial diversity and anaerobic hydrocarbon degradation potential in an oil-contaminated mangrove sediment. BMC Microbiol 12(1):186.  https://doi.org/10.1186/1471-2180-12-186 CrossRefGoogle Scholar
  2. Baldrian P (2006) Fungal laccases occurrence and properties. FEMS Microbiol Rev 30:215–242.  https://doi.org/10.1111/j.1574-4976.2005.00010.x CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. Birkigt J, Gilevska T, Ricken B, Richnow HH, Vione D, Corvini PF, Nijenhuis I, Cichocka D (2015) Carbon stable isotope fractionation of sulfamethoxazole during biodegradation by Microbacterium sp. strain BR1 and upon direct photolysis. Environ Sci Technol 49(10):6029–6036.  https://doi.org/10.1021/acs.est.5b00367 CrossRefGoogle Scholar
  5. Castillo-Carvajal LC, Sanz-Martín JL, Barragán-Huerta BE (2014) Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review. Environ Sci Pollut Res 21(16):9578–9588.  https://doi.org/10.1007/s11356-014-3036-z CrossRefGoogle Scholar
  6. Chang BV, Lu ZJ, Yuan SY (2009) Anaerobic degradation of nonylphenol in subtropical mangrove sediments. J Hazard Mater 165(1-3):162–167.  https://doi.org/10.1016/j.jhazmat.2008.09.085 CrossRefGoogle Scholar
  7. Chang BV, Ren YL (2015) Biodegradation of three tetracyclines in river sediment. Ecol Eng 75:272–277.  https://doi.org/10.1016/j.ecoleng.2014.11.039 CrossRefGoogle Scholar
  8. Chen Q, Li J, Liu M, Sun H, Bao M (2017) Study on the biodegradation of crude oil by free and immobilized bacterial consortium in marine environment. PLoS ONE 12:e0174445.  https://doi.org/10.1371/journal.pone.0174445 CrossRefGoogle Scholar
  9. 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(17):9566–9575.  https://doi.org/10.1021/acs.est.6b02231 CrossRefGoogle Scholar
  10. Fenu A, Donckels BM, 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(10):1754–1761.  https://doi.org/10.2166/wst.2015.397 CrossRefGoogle Scholar
  11. Gui M, Chen Q, Ni J (2017) Effect of sulfamethoxazole on aerobic denitrification by strain Pseudomonas stutzeri PCN-1. Bioresour Technol 235:325–331.  https://doi.org/10.1016/j.biortech.2017.03.131 CrossRefGoogle Scholar
  12. Herzog B, Lemmer H, Horn H, Müller E (2013) Characterization of pure cultures isolated from sulfamethoxazole-acclimated activated sludge with respect to taxonomic identification and sulfamethoxazole biodegradation potential. BMC Microbiol 13(1):276.  https://doi.org/10.1186/1471-2180-13-276 CrossRefGoogle Scholar
  13. Hsu FY, Wang ZY, Chang BV (2013) Use of microcapsules with electrostatically immobilized bacterial cells or enzyme extract to remove nonylphenol in wastewater sludge. Chemosphere 91(6):745–750.  https://doi.org/10.1016/j.chemosphere.2013.02.019 CrossRefGoogle Scholar
  14. 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(1):140–151.  https://doi.org/10.1007/s00248-012-0010-5 CrossRefGoogle Scholar
  15. 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(10):4671–4681.  https://doi.org/10.1007/s00253-013-5488-3 CrossRefGoogle Scholar
  16. Lai HT, Wang TS, Chou CC (2011) Implication of light sources and microbial activities on degradation of sulfonamides in water and sediment from a marine shrimp pond. Bioresour Technol 102(8):5017–5023.  https://doi.org/10.1016/j.biortech.2011.01.070 CrossRefGoogle Scholar
  17. Larcher S, Yargeau V (2011) Biodegradation of sulfamethoxazole by individual and mixed bacteria. Appl Microbiol Biotechnol 91(1):211–218.  https://doi.org/10.1007/s00253-011-3257-8 CrossRefGoogle Scholar
  18. Larcher S, Yargeau V (2012) Biodegradation of sulfamethoxazole: current knowledge and perspectives. Appl Microbiol Biotechnol 96(2):309–318.  https://doi.org/10.1007/s00253-012-4326-3 CrossRefGoogle Scholar
  19. Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52(9):1539–1546.  https://doi.org/10.1016/S0045-6535(03)00493-4 CrossRefGoogle Scholar
  20. Lee SM, Koo BW, Lee SS, Kim MK, Choi DH, Hong EJ, Jeung EB, Choi IG (2004) Biodegradation of dibutyl phthalate by white rot fungi and evaluation on its estrogenic activity. Enzyme Microb Technol 35(5):417–423.  https://doi.org/10.1016/j.enzmictec.2004.06.001 CrossRefGoogle Scholar
  21. Lei X, Lu J, Liu Z, Tong Y, Li S (2015) Concentration and distribution of antibiotics in water-sediment system of Bosten Lake, Xinjiang. Environ Sci Pollut Res 22(3):1670–1678.  https://doi.org/10.1007/s11356-014-2994-5 CrossRefGoogle Scholar
  22. Li X, Xu QM, Cheng JS, Yuan YJ (2016) Improving the bioremoval of sulfamethoxazole and alleviating cytotoxicity of its biotransformation by laccase producing system under coculture of Pycnoporus sanguineus and Alcaligenes faecalis. Bioresour Technol 220:333–340.  https://doi.org/10.1016/j.biortech.2016.08.088 CrossRefGoogle Scholar
  23. Li XZ, Lin XG, Zhang J, Wu YC, Yin R, Feng YZ, Wang Y (2010) Degradation of polycyclic aromatic hydrocarbons by crude extracts from spent mushroom substrate and its possible mechanisms. Curr Microbiol 60:336–342.  https://doi.org/10.1007/s00284-009-9546-0 CrossRefGoogle Scholar
  24. Li Z, Chang Q, Li S, Gao M, She Z, Guo L, Zhao Y, Jin C, Zheng D, Xu Q (2017) Impact of sulfadiazine on performance and microbial community of a sequencing batch biofilm reactor treating synthetic mariculture wastewater. Bioresour Technol 235:122–130.  https://doi.org/10.1016/j.biortech.2017.03.113 CrossRefGoogle Scholar
  25. Lin AY, Yu TH, Lin CF (2008) Pharmaceutical contamination in residential, industrial, and agricultural waste streams: risk to aqueous environments in Taiwan. Chemosphere 74(1):131–141.  https://doi.org/10.1016/j.chemosphere.2008.08.027 CrossRefGoogle Scholar
  26. Mulla SI, Sun Q, Hu A, Wang Y, Ashfaq M, Eqani SA, Yu CP (2016) Evaluation of sulfadiazine degradation in three newly isolated pure bacterial cultures. PLoS One 11(10):e0165013.  https://doi.org/10.1371/journal.pone.0165013 CrossRefGoogle Scholar
  27. Pepper LL, Gerba CP, Gentry TJ (2015) Environmental microbiology. In: Maier MM, Gentry TJ (eds) Microorganisms and organic pollutants. Elsevier Inc., CA, pp 377–413Google Scholar
  28. Reis PJ, Reis AC, Ricken B, Kolvenbach BA, Manaia CM, Corvini PF, 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 CrossRefGoogle Scholar
  29. Tam NF, Guo CL, Yau WY, Wong YS (2002) Preliminary study on biodegradation of phenanthrene by bacteria isolated from mangrove sediments in Hong Kong. Mar Pollut Bull 45(1-12):316–324.  https://doi.org/10.1016/S0025-326X(02)00108-X CrossRefGoogle Scholar
  30. Tamtam F, Mercier F, Le Bot B, Eurin J, Tuc Dinh Q, Clément M, Chevreuil M (2008) Occurrence and fate of antibiotics in the Seine River in various hydrological conditions. Sci Total Environ 393(1):84–95.  https://doi.org/10.1016/j.scitotenv.2007.12.009 CrossRefGoogle Scholar
  31. Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166(2):145–167.  https://doi.org/10.1002/jpln.200390023 CrossRefGoogle Scholar
  32. Walker N (1978) A soil Flavobacterium sp. that degrades sulphanilamide and asulam. J Appl Bacteriol 45(1):125–129.  https://doi.org/10.1111/j.1365-2672.1978.tb04205.x CrossRefGoogle Scholar
  33. Yan N, Xia S, Xu L, Zhu J, Zhang Y, Rittmann BE (2012) Internal loop photobiodegradation reactor (ILPBR) for accelerated degradation of sulfamethoxazole (SMX). Appl Microbiol Biotechnol 94(2):527–535.  https://doi.org/10.1007/s00253-011-3742-0 CrossRefGoogle Scholar
  34. Yang CW, Huang HW, Chao WL, Chang BV (2015) Bacterial communities associated with aerobic degradation of polybrominated diphenyl ethers from river sediments. Environ Sci Pollut Res 22(5):3810–3819.  https://doi.org/10.1007/s11356-014-3626-9 CrossRefGoogle Scholar
  35. Yang CW, Hsiao WC, Chang BV (2016) Biodegradation of sulfonamide antibiotics in sludge. Chemosphere 150:559–565.  https://doi.org/10.1016/j.chemosphere.2016.02.064 CrossRefGoogle Scholar
  36. Yang CW, Lee CC, Ku H, Chang BV (2017) Bacterial communities associated with anaerobic debromination of decabromodiphenyl ether from mangrove sediment. Environ Sci Pollut Res 24(6):5391–5403.  https://doi.org/10.1007/s11356-016-8259-8 CrossRefGoogle Scholar
  37. Yu SH, Ke L, Wong YS, Tam NF (2005) Degradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. Environ Int 31(2):149–154.  https://doi.org/10.1016/j.envint.2004.09.008 CrossRefGoogle Scholar
  38. Yuan SY, Huang IC, Chang BV (2010) Biodegradation of dibutyl phthalate and di-(2-ethylhexyl) phthalate and microbial community changes in mangrove sediment. J Hazard Mater 184(1-3):826–831.  https://doi.org/10.1016/j.jhazmat.2010.08.116 CrossRefGoogle Scholar
  39. 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 Microbiol Biotechnol 28(2):447–452.  https://doi.org/10.1007/s11274-011-0834-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of MicrobiologySoochow UniversityTaipeiTaiwan

Personalised recommendations