Degradation of Erythromycin by a Novel Fungus, Penicillium oxalicum RJJ-2, and the Degradation Pathway

Abstract

Purpose

This study aimed to isolate effective erythromycin-degrading fungi and determine the characteristics and pathway of degradation.

Methods

Erythromycin-degrading fungi were isolated from erythromycin-contaminated samples using a standard enrichment and isolation method. The degradation characteristics were investigated in mineral salt medium (MSM) with erythromycin as a sole carbon source. Key degradation intermediates were analyzed by high performance liquid chromatography–mass spectrometry (HPLC–MS) and used to deduce the erythromycin degradation pathway of strain RJJ-2.

Results

A novel erythromycin-degrading fungus RJJ-2, was isolated from a contaminated sample. Based on its morphology and internal transcribed spacer (ITS) sequence, the strain was 100% similar to P. oxalicum (MN759650) and named P. oxalicum RJJ-2. The strain RJJ-2 degraded 84.88% erythromycin after 96-h incubation at 35 °C and pH 6.0 in MSM with erythromycin (100 mg L−1) as the sole carbon source. Optimal degradation conditions for P. oxalicum RJJ-2 were 35 °C, and pH 6.0 with 0.1% ammonium sulfate supplementation. HPLC–MS analysis indicated that the main degradation intermediates were 3-depyranosyloxy erythromycin A, cladinose, desosamine, and 7,12-dyhydroxy-6-deoxyerythronolide B. It was inferred that the erythromycin was degraded to 3-depyranosyloxy erythromycin A by a glycoside hydrolase in the initial reaction.

Conclusion

This study demonstrated that P. oxalicum RJJ-2 is a novel erythromycin-degrading strain, which can provide a new eco-friendly and cost-effective approach for the disposal of erythromycin fermentation wastes and other hazardous chemicals.

Graphic Abstract

This is a preview of subscription content, access via your institution.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

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

Abbreviations

PCR:

Polymerase chain reaction

HPLC–MS:

High performance liquid chromatography–mass spectrometry

AFWs:

Antibiotic fermentation wastes

ITS:

Internal transcribed spacer

References

  1. 1.

    Chu, L., Chen, D., Wang, J., Yang, Z., Shen, Y.: Degradation of antibiotics and antibiotic resistance genes in erythromycin fermentation residues using radiation coupled with peroxymonosulfate oxidation. Waste Manage. 96, 190–197 (2019). https://doi.org/10.1016/j.wasman.2019.07.031

    Article  Google Scholar 

  2. 2.

    Klein, E.Y., Van Boeckel, T.P., Martinez, E.M., Pant, S., Gandra, S., Levin, S.A., Goossens, H., Laxminarayan, R.: Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc. Natl. Acad. Sci. USA 115(15), E3463–E3470 (2018)

    Article  Google Scholar 

  3. 3.

    Shen, Y., Chu, L., Zhuan, R., Xiang, X., Sun, H., Wang, J.: Degradation of antibiotics and antibiotic resistance genes in fermentation residues by ionizing radiation: a new insight into a sustainable management of antibiotic fermentative residuals. J Environ. Manage. 232, 171–178 (2019). https://doi.org/10.1016/j.jenvman.2018.11.050

    Article  Google Scholar 

  4. 4.

    Ma, D., Zhang, G., Areeprasert, C., Li, C., Shen, Y., Yoshikawa, K.: Characterization of NO emission in combustion of hydrothermally treated antibiotic mycelial residue. Chem. Eng. J. 284, 708–715 (2016)

    Article  Google Scholar 

  5. 5.

    Tang, R., Yuan, S., Chen, F., Zhan, X., Wang, W., Hu, Z.: Effects of roxarsone and sulfadiazine on biogas production and their degradation during anaerobic digestion. Int. Biodeterior. Biodegradation 140, 113–118 (2019). https://doi.org/10.1016/j.ibiod.2019.04.001

    Article  Google Scholar 

  6. 6.

    Sun, Q., Bai, Y., Zhao, C., Xiao, Y., Wen, D., Tang, X.: Aerobic biodegradation characteristics and metabolic products of quinoline by a Pseudomonas strain. Biores. Technol. 100(21), 5030–5036 (2009). https://doi.org/10.1016/j.biortech.2009.05.044

    Article  Google Scholar 

  7. 7.

    Liao, H., Zhao, Q., Cui, P., Chen, Z., Yu, Z., Geisen, S., Friman, V.P., Zhou, S.: Efficient reduction of antibiotic residues and associated resistance genes in tylosin antibiotic fermentation waste using hyperthermophilic composting. Environ. Int. 133, 105203 (2019). https://doi.org/10.1016/j.envint.2019.105203

    Article  Google Scholar 

  8. 8.

    Cizmek, L., Sabic, M., Mestrovic, E., Domanovac, M.: Biodegradation of Erythromycin with Environmental Microorganism Pseudomonas aeruginosa 3011. Chem. Biochem. Eng. Q. 29, 367–373 (2015)

    Article  Google Scholar 

  9. 9.

    Zhang, W., Qiu, L., Gong, A., Yuan, X.: Isolation and characterization of a high-efficiency erythromycin A-degrading Ochrobactrum sp. strain. Marine Pollut. Bull. 114(2), 896–902 (2017). https://doi.org/10.1016/j.marpolbul.2016.10.076

    Article  Google Scholar 

  10. 10.

    Kim, H.E., Park, K.R.: Purification and Characterization of an Esterase from Acinetobacter lwoffii I6C–1. Curr. Microbiol. 44(6), 401–405 (2002)

    Article  Google Scholar 

  11. 11.

    Wen, X., Jia, Y., Li, J.: Enzymatic degradation of tetracycline and oxytetracycline by crude manganese peroxidase prepared from Phanerochaete chrysosporium. J. Hazard. Mater. 177(1–3), 924–928 (2010). https://doi.org/10.1016/j.jhazmat.2010.01.005

    Article  Google Scholar 

  12. 12.

    Buchicchio, A., Bianco, G., Sofo, A., Masi, S., Caniani, D.: Biodegradation of carbamazepine and clarithromycin by Trichoderma harzianum and Pleurotus ostreatus investigated by liquid chromatography–high-resolution tandem mass spectrometry (FTICR MS-IRMPD). Sci. Total Environ. 557–558(Jul 1), 733–739 (2016)

    Article  Google Scholar 

  13. 13.

    Olicon-Hernandez, D.R., Camacho-Morales, R.L., Pozo, C., Gonzalez-Lopez, J., Aranda, E.: Evaluation of diclofenac biodegradation by the ascomycete fungus Penicillium oxalicum at flask and bench bioreactor scales. Sci. Total Environ. 662, 607–614 (2019). https://doi.org/10.1016/j.scitotenv.2019.01.248

    Article  Google Scholar 

  14. 14.

    Caniani, D., Caivano, M., Pascale, R., Bianco, G., Mancini, I.M., Masi, S., Mazzone, G., Firouzian, M., Rosso, D.: CO2 and N2O from water resource recovery facilities: evaluation of emissions from biological treatment, settling, disinfection, and receiving water body. Sci. Total Environ. 648, 1130–1140 (2019). https://doi.org/10.1016/j.scitotenv.2018.08.150

    Article  Google Scholar 

  15. 15.

    Birolli, W.G., Vacondio, B., Alvarenga, N., Seleghim, M.H.R., Porto, A.L.M.: Enantioselective biodegradation of the pyrethroid (+/-)-lambda-cyhalothrin by marine-derived fungi. Chemosphere 197, 651–660 (2018). https://doi.org/10.1016/j.chemosphere.2018.01.054

    Article  Google Scholar 

  16. 16.

    Ren, J., Fan, B., Huhetaoli, N., Niu, D., Gu, Y., Li, C.: Biodegradation of waste cooking oils by Klebsiella quasivariicola IUMR-B53 and characteristics of its oil-degrading enzyme. Waste Biomass Valoriz. (2020). https://doi.org/10.1007/s12649-020-01097-z

    Article  Google Scholar 

  17. 17.

    Zuo, S.S., Niu, D.Z., Ning, T.T., Zheng, M.L., Jiang, D., Xu, C.C.: Protein enrichment of sweet potato beverage residues mixed with peanut shells by Aspergillus oryzae and Bacillus subtilis using central composite design. Waste Biomass Valoriz. 9(5), 835–844 (2017). https://doi.org/10.1007/s12649-017-9844-x

    Article  Google Scholar 

  18. 18.

    Liu, M., Feng, P., Kakade, A., Yang, L., Chen, G., Yan, X., Ni, H., Liu, P., Kulshreshtha, S., Abomohra, A.E., Li, X.: Reducing residual antibiotic levels in animal feces using intestinal Escherichia coli with surface-displayed erythromycin esterase. J. Hazard. Mater. 388, 122032 (2020). https://doi.org/10.1016/j.jhazmat.2020.122032

    Article  Google Scholar 

  19. 19.

    Ding, T., Zhou, Y., Qin, J.J., Yang, L.J., Zhang, W.D., Shen, Y.H.: Chemical constituents from wetland soil fungus Penicillium oxalicum GY1. Fitoterapia 142, 104530 (2020). https://doi.org/10.1016/j.fitote.2020.104530

    Article  Google Scholar 

  20. 20.

    Li, F., Yu, D., Lin, X., Liu, D., Xia, H., Chen, S.: Biodegradation of poly(epsilon-caprolactone) (PCL) by a new Penicillium oxalicum strain DSYD05-1. World J. Microbiol. Biotechnol. 28(10), 2929–2935 (2012). https://doi.org/10.1007/s11274-012-1103-5

    Article  Google Scholar 

  21. 21.

    Pareek, N., Vivekanand, V., Dwivedi, P., Singh, R.P.: Penicillium oxalicum SAEM-51: a mutagenised strain for enhanced production of chitin deacetylase for bioconversion to chitosan. New Biotechnol. 28(2), 118–124 (2011). https://doi.org/10.1016/j.nbt.2010.09.009

    Article  Google Scholar 

  22. 22.

    Satti, S.M., Shah, Z., Luqman, A., Hasan, F., Osman, M., Shah, A.A.: Biodegradation of poly(3-hydroxybutyrate) and poly(3-hydroxybutyrate-co-3-hydroxyvalerate) by newly isolated Penicillium oxalicum SS2 in soil microcosms and partial characterization of extracellular depolymerase. Curr. Microbiol. (2020). https://doi.org/10.1007/s00284-020-01968-7

    Article  Google Scholar 

  23. 23.

    Tian, H., Ma, Y.J., Li, W.Y., Wang, J.W.: Efficient degradation of triclosan by an endophytic fungus Penicillium oxalicum B4. Environ. Sci. Pollut. Res. Int. 25(9), 8963–8975 (2018). https://doi.org/10.1007/s11356-017-1186-5

    Article  Google Scholar 

  24. 24.

    Fan, C., He, J.: Proliferation of antibiotic resistance genes in microbial consortia of sequencing batch reactors (SBRs) upon exposure to trace erythromycin or erythromycin-H2O. Water Res. 45(10), 1–3106 (2011)

    Article  Google Scholar 

  25. 25.

    Mao, F., Liu, C., He, M., Shi, W., Xue, G., Gao, P.: Isolation and identification of an erythromycin degradation bacterium and study on its biodegradation characteristics. Environ. Sci. Technol. 36(7), 9–12 (2013)

    Google Scholar 

  26. 26.

    Akbar, S., Hasan, F., Nadhman, A., Khan, S., Shah, A.A.: Production and purification of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) degrading enzyme from Streptomyces sp. AF-111. J. Polym. Environ. 21(4), 1109–1116 (2013)

    Article  Google Scholar 

  27. 27.

    Feng, W., Wei, Z., Song, J., Qin, Q., Yu, K., Li, G., Zhang, J., Wu, W., Yan, Y.: Hydrolysis of nicosulfuron under acidic environment caused by oxalate secretion of a novel Penicillium oxalicum strain YC-WM1. Sci. Rep. 7(1), 647 (2017). https://doi.org/10.1038/s41598-017-00228-2

    Article  Google Scholar 

  28. 28.

    Morar, M., Pengelly, K., Koteva, K., Wright, G.D.: Mechanism and diversity of the erythromycin esterase family of enzymes. Biochemistry 51(8), 1740–1751 (2012). https://doi.org/10.1021/bi201790u

    Article  Google Scholar 

  29. 29.

    Olicón-Hernández, D.R., Jesús, G.L., Elisabet, A.: Overview on the biochemical potential of filamentous fungi to degrade pharmaceutical compounds. Front. Microbiol. 8, 1792 (2017)

    Article  Google Scholar 

  30. 30.

    Hansen, L.H., Mauvais, P., Douthwaite, S.: The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23 S ribosomal RNA. Mol Microbiol 31, 623–631 (1999)

    Article  Google Scholar 

Download references

Acknowledgements

This study was financially supported by Yili Chuanning Biotechnology Co., Ltd. (Grant Nos. 2019K1238 and 2019K1237); Hebei Cixin Environmental Technology Co., Ltd. China. (Grant No. 2018K0948); Shaanxi Xintiandi Grass Industry Co., Ltd. China. (Grant No. 2018K0947); Research on the Development Strategy of Bioenergy and Geothermal Energy Engineering Science and Technology for 2035 (Grant No. 2019-ZCQ-04) and Science Foundation of Changzhou University (Grant No. ZMF18020316).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Chunyu Li.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ren, J., Wang, Z., Deng, L. et al. Degradation of Erythromycin by a Novel Fungus, Penicillium oxalicum RJJ-2, and the Degradation Pathway. Waste Biomass Valor (2021). https://doi.org/10.1007/s12649-021-01343-y

Download citation

Keywords

  • Biodegradation
  • Degradation pathway
  • Erythromycin
  • Penicillium oxalicum