Replacement of Soybean Meal with Animal Origin Protein Meals Improved Ramoplanin A2 Production by Actinoplanes sp. ATCC 33076

Abstract

Ramoplanin A2 is the last resort antibiotic for treatment of many high morbidity- and mortality-rated hospital infections, and it is expected to be marketed in the forthcoming years. Therefore, high-yield production of ramoplanin A2 gains importance. In this study, meat-bone meal, poultry meal, and fish meal were used instead of soybean meal for ramoplanin A2 production by Actinoplanes sp. ATCC 33076. All animal origin nitrogen sources stimulated specific productivity. Ramoplanin A2 levels were determined as 406.805 mg L−1 in fish meal medium and 374.218 mg L−1 in poultry meal medium. These levels were 4.25- and 4.09-fold of basal medium, respectively. However, the total yield of poultry meal was higher than that of fish meal, which is also low-priced. In addition, the variations in pH levels, protein levels, reducing sugar levels, extracellular protease, amylase and lipase activities, and intracellular free amino acid levels were monitored during the incubation period. The correlations between ramoplanin production and these variables with respect to the incubation period were determined. The intracellular levels of l-Phe, d-Orn, and l-Leu were found critical for ramoplanin A2 production. The strategy of using animal origin nitrogen sources can be applied for large-scale ramoplanin A2 production.

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References

  1. 1.

    Hancock, R. E. (2005). Mechanisms of action of newer antibiotics for gram-positive pathogens. The Lancet Infectious Diseases, 5(4), 209–218.

    CAS  Article  Google Scholar 

  2. 2.

    Yin, X. (2014). Formulations combining ramoplanin and rhamnolipids for combating bacterial infection. United States Patent Application Publication, US 20140294925 A1.

  3. 3.

    Emerson, C. R., & Marzella, N. (2007). Ramoplanin: a promising treatment option for Clostridium difficile-associated diarrhea and vancomycin-resistant Enterococcus. Drug Forecast, 32, 541–543.

    Google Scholar 

  4. 4.

    Pelaez, T., Alcala, L., Alonso, R., Martín-López, A., García-Arias, V., Marín, M., & Bouza, E. (2005). In vitro activity of ramoplanin against Clostridium difficile, including strains with reduced susceptibility to vancomycin or with resistance to metronidazole. Antimicrobial Agents and Chemotherapy, 49(3), 1157–1159.

    CAS  Article  Google Scholar 

  5. 5.

    Huang, H., Weintraub, A., Fang, H., & Nord, C. E. (2009). Antimicrobial resistance in Clostridium difficile. International Journal of Antimicrobial Agents, 34(6), 516–522.

    CAS  Article  Google Scholar 

  6. 6.

    Steinkämper, A., Schmid, J., Schwartz, D., & Biener, R. (2015). Development of cultivation strategies for friulimicin production in Actinoplanes friuliensis. Journal of Biotechnology, 195, 52–59.

    Article  Google Scholar 

  7. 7.

    Schmidt, J. W., Greenough, A., Burns, M., Luteran, A. E., & McCafferty, D. G. (2010). Generation of ramoplanin-resistant Staphylococcus aureus. FEMS Microbiology Letters, 310(2), 104–111.

    CAS  Article  Google Scholar 

  8. 8.

    McCafferty, D. G., Cudic, P., Frankel, B. A., Barkallah, S., Kruger, R. G., & Li, W. (2002). Chemistry and biology of the ramoplanin family of peptide antibiotics. Biopolymers, 66(4), 261–84.

    CAS  Article  Google Scholar 

  9. 9.

    Hamedi, J., Imanparast, F., Tirandaz, H., Laamerad, B., & Sadrai, S. (2012). Improvement of clavulanic acid production by Streptomyces clavuligerus with peanut derivatives. Annals of Microbiology, 62(3), 1227–1234.

    CAS  Article  Google Scholar 

  10. 10.

    Zou, X., Hang, H. F., Chu, J., Zhuang, Y. P., & Zhang, S. L. (2009). Enhancement of erythromycin A production with feeding available nitrogen sources in erythromycin biosynthesis phase. Bioresource Technology, 100(13), 3358–3365.

    CAS  Article  Google Scholar 

  11. 11.

    Vázquez, J. A., González, M., & Murado, M. A. (2004). Peptones from autohydrolysed fish viscera for nisin and pediocin production. Journal of Biotechnology, 112(3), 299–311.

    Article  Google Scholar 

  12. 12.

    Cavalleri, B., Pagani, H., Volpe, G., Selva, E., & Parenti, F. (1984). A-16686, a new antibiotic from Actinoplanes I. fermentation, isolation and preliminary physico-chemical characteristics. The Journal of Antibiotics, 37(4), 309–317.

    CAS  Article  Google Scholar 

  13. 13.

    Brunati, M., Bava, A., Marinelli, F., & Lancini, G. (2005). Influence of leucine and valine on ramoplanin production by Actinoplanes sp. ATCC 33076. The Journal of Antibiotics, 58(7), 473–478.

    CAS  Article  Google Scholar 

  14. 14.

    Restelli, E. & Mainoli, L. (1996). Antibiotic A/16686 recovery process. European Patent Office, EP 0427142 A1.

  15. 15.

    Jámbor, A., & Molnár-Perl, I. (2009). Amino acid analysis by high-performance liquid chromatography after derivatization with 9-fluorenylmethyloxycarbonyl chloride: literature overview and further study. Journal of Chromatography A, 1216(15), 3064–3077.

    Article  Google Scholar 

  16. 16.

    Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.

    CAS  Article  Google Scholar 

  17. 17.

    Miller, G. L. (1959). Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry, 31(3), 426–428.

    CAS  Article  Google Scholar 

  18. 18.

    Kembhavi, A. A., Buttle, D. J., Knight, C. G., & Barrett, A. J. (1993). The two cysteine endopeptidases of legume seeds: purification and characterization by use of specific fluorometricassays. Archives of Biochemistry and Biophysics, 303(2), 208–213.

    CAS  Article  Google Scholar 

  19. 19.

    Grbavčić, S., Bezbradica, D., Izrael-Živković, L., Avramović, N., Milosavić, N., Karadžić, I., & Knežević-Jugović, Z. (2011). Production of lipase and protease from an indigenous Pseudomonas aeruginosa strain and their evaluation as detergent additives: compatibility study with detergent ingredients and washing performance. Bioresource Technology, 102(24), 11226–11233.

    Article  Google Scholar 

  20. 20.

    Sapkota, A.R., Lefferts, L.Y., McKenzie, S. & Walker, P. (2007). What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. Environmental Health Perspectives, 663–670.

  21. 21.

    Darah, I., Nur-Diyana, A., Nurul-Husna, S., Jain, K., & Lim, S. H. (2013). Microsporum fulvum IBRL SD3: as novel isolate for chicken feathers degradation. Applied Biochemistry and Biotechnology, 171(7), 1900–1910.

    CAS  Article  Google Scholar 

  22. 22.

    Esakkiraj, P., Dhas, G. A. J., Palavesam, A., & Immanuel, G. (2010). Media preparation using tuna-processing wastes for improved lipase production by shrimp gut isolate Staphylococcus epidermidis CMST Pi 2. Applied Biochemistry and Biotechnology, 160(4), 1254–1265.

    CAS  Article  Google Scholar 

  23. 23.

    Forgács, G., Lundin, M., Taherzadeh, M. J., & Horváth, I. S. (2013). Pretreatment of chicken feather waste for improved biogas production. Applied Biochemistry and Biotechnology, 169(7), 2016–2028.

    Article  Google Scholar 

  24. 24.

    Serrano, A., Siles, J. A., Gutiérrez, M. C., & Martín, M. Á. (2014). Optimization of anaerobic co-digestion of strawberry and fish waste. Applied Biochemistry and Biotechnology, 173(6), 1391–1404.

    CAS  Article  Google Scholar 

  25. 25.

    Centenaro, G. S., Salas-Mellado, M., Pires, C., Batista, I., Nunes, M. L., & Prentice, C. (2014). Fractionation of protein hydrolysates of fish and chicken using membrane ultrafiltration: investigation of antioxidant activity. Applied Biochemistry and Biotechnology, 172(6), 2877–2893.

    CAS  Article  Google Scholar 

  26. 26.

    Godinho, I., Pires, C., Pedro, S., Teixeira, B., Mendes, R., Nunes, M.L. & Batista, I. (2015). Antioxidant properties of fish protein hydrolysates prepared from cod protein hydrolysate by Bacillus sp. Applied Biochemistry and Biotechnology, 118.

  27. 27.

    Farver, D. K., Hedge, D. D., & Lee, S. C. (2005). Ramoplanin: a lipoglycodepsipeptide antibiotic. Annals of Pharmacotherapy, 39(5), 863–868.

    CAS  Article  Google Scholar 

  28. 28.

    Xiangjin, W. U., Xiangjing, W. A. N. G., Yingzi, S. H. I., Wensheng, X. I. A. N. G., & Hua, B. A. I. (2008). Improvement of ramoplanin production by mutation and medium optimization. Journal of Northeast Agricultural University, 15(1), 18–22.

    Google Scholar 

  29. 29.

    Kayali, H. A., Tarhan, L., Sazak, A., & Şahin, N. (2011). Carbohydrate metabolite pathways and antibiotic production variations of a novel Streptomyces sp. M3004 depending on the concentrations of carbon sources. Applied Biochemistry and Biotechnology, 165(1), 369–381.

    CAS  Article  Google Scholar 

  30. 30.

    Li, M., Chen, S., Li, J., & Ji, Z. (2014). Propanol addition improves natamycin biosynthesis of Streptomyces natalensis. Applied Biochemistry and Biotechnology, 172(7), 3424–3432.

    CAS  Article  Google Scholar 

  31. 31.

    Yang, Y. H., Song, E., Kim, E. J., Lee, K., Kim, W. S., Park, S. S., & Kim, B. G. (2009). NdgR, an IclR-like regulator involved in amino-acid-dependent growth, quorum sensing, and antibiotic production in Streptomyces coelicolor. Applied Microbiology and Biotechnology, 82(3), 501–511.

    CAS  Article  Google Scholar 

  32. 32.

    Sánchez, C., Gómez, N., Quintero, J.C., Ochoa, S. & Rios, R. (2014). A combined sensitivity and metabolic flux analysis unravel the importance of amino acid feeding strategies in clavulanic acid biosynthesis. In Advances in Computational Biology, (pp. 169–175). Springer International Publishing.

  33. 33.

    Saudagar, P. S., & Singhal, R. S. (2007). Optimization of nutritional requirements and feeding strategies for clavulanic acid production by Streptomyces clavuligerus. Bioresource Technology, 98(10), 2010–2017.

    CAS  Article  Google Scholar 

  34. 34.

    Chen, K. C., Lin, Y. H., Wu, J. Y., & Hwang, S. C. J. (2003). Enhancement of clavulanic acid production in Streptomyces clavuligerus with ornithine feeding. Enzyme and Microbial Technology, 32(1), 152–156.

    Article  Google Scholar 

  35. 35.

    Song, J. M., Park, J. T., Lee, H. S., Kang, J. H., & Kang, D. J. (2008). Production of teicoplanin from Actinoplanes teichomyceticus ID9303 by adding proline. Bioscience, Biotechnology, and Biochemistry, 72(6), 1635–1637.

    CAS  Article  Google Scholar 

  36. 36.

    Borghi, A., Edwards, D., Zerilli, L. F., & Lancini, G. C. (1991). Factors affecting the normal and branched-chain acyl moieties of teicoplanin components produced by Actinoplanes teichomyceticus. Journal of General Microbiology, 137(3), 587–592.

    CAS  Article  Google Scholar 

  37. 37.

    Zou, X., Li, W. J., Zeng, W., Chu, J., Zhuang, Y. P., & Zhang, S. L. (2011). An assessment of seed quality on erythromycin production by recombinant Saccharopolyspora erythraea strain. Bioresource Technology, 102(3), 3360–3365.

    CAS  Article  Google Scholar 

  38. 38.

    Kim, H. S., & Park, Y. I. (2007). Lipase activity and tacrolimus production in Streptomyces clavuligerus CKD 1119 mutant strains. Journal of Microbiology and Biotechnology, 17(10), 1638–1644.

    CAS  Google Scholar 

  39. 39.

    Ayar-Kayali, H., & Tarhan, L. (2006). Vancomycin antibiotic production and TCA-glyoxalate pathways depending on the glucose concentration in Amycolatopsis orientalis. Enzyme and Microbial Technology, 38(6), 727–734.

    CAS  Article  Google Scholar 

Download references

Acknowledgments

The study was financially supported by a Grant from Dokuz Eylul University Department of Scientific Research Projects (project number: 2015.KB.FEN.009).

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Correspondence to Hulya Ayar Kayali.

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Erkan, D., Kayali, H.A. Replacement of Soybean Meal with Animal Origin Protein Meals Improved Ramoplanin A2 Production by Actinoplanes sp. ATCC 33076. Appl Biochem Biotechnol 180, 306–321 (2016). https://doi.org/10.1007/s12010-016-2100-1

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Keywords

  • Ramoplanin A2 production
  • Soybean meal
  • Meat-bone meal
  • Poultry meal
  • Fish meal