Tuna Condensate Waste with Molasses as a Renewable Substrate for Antifungal Compounds by Streptomyces philanthi RL-1-178 Against Aflatoxingenic B1 (AFB1) Aspergillus flavus

Abstract

This study aims to utilize tuna condensate as a renewable resource for production of antifungal compounds by Streptomyces philanthi RL-1-178 against aflatoxingenic B1 (AFB1) Aspergillus flavus. Among ten isolates of A. flavus tested, the strain PSRDC-4 was the most toxigenic strain (1432 ppb of AFB1) and aggressive to S. philanthi (85.9% inhibition). The effective dose (100% inhibition) of the culture filtrate RL-1-178 was at 10.0% (v/v) with 1 h exposure time. The antifungal compounds, identified by GC–MS analysis, were consisted of 105 components with 2,4-imidazolidinedione (31.2%) followed by acetic acid (25.27%) was the most abundant. The optimum condition for growth and production of antifungal compounds from S. philanthi RL-1-178 was as following; tuna condensate of 15,000 mg L−1 COD, the initial pH at 7.0, incubation temperature at 30 °C and supplemented with 8 g L−1 of molasses. Therefore, tuna condensate exhibited a high potential to be utilized as an alternative medium for antifungal production by S. philanthi RL-1-178.

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

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

References

  1. 1.

    Prasertsan, P., Choorit, W.: Problem and solution of the occurrence of red colour in wastewater of seafood processing plant. Songklanakarin J. Sci. Technol. 10, 439–446 (1988)

    Google Scholar 

  2. 2.

    Prasertsan, P., Choorit, W., Suwanno, S.: Optimisation for growth of Rhodocyclus gelatinosus in seafood processing effluents. World J. Microbiol. Biotechnol. 9, 593–596 (1993)

    Google Scholar 

  3. 3.

    Sarabok, A., H-Kittikun, A.: Enzymatic hydrolysis of tuna condensate for flavour sauce production. Songklanakarin J. Sci. Technol. 21, 291–500 (1999)

    Google Scholar 

  4. 4.

    Prasertsan, P., Jaturapornpipat, M., Siripatana, C.: Utilization and treatment of tuna condensate by photosynthetic bacteria. Pure Appl. Chem. 69, 2439–2445 (1997)

    Google Scholar 

  5. 5.

    Azad, S.A., Vikineswary, S., Chong, V.C., Ramachandran, K.B.: Rhodovulum sulfidophilum in the treatment and utilization of sardine processing wastewater. Lett. Appl. Microbiol. 38, 13–18 (2004)

    Google Scholar 

  6. 6.

    Saimmai, A., Sobhon, V., Maneerat, S.: Molasses as a whole medium for biosurfactants production by Bacillus strains and their application. Appl. Biochem. Biotechnol. 165, 315–335 (2011)

    Google Scholar 

  7. 7.

    Płaza, G.A., Turek, A., Król, E., Szczygłowska, R.: Antifungal and antibacterial properties of surfactin isolated from Bacillus subtilis growing on molasses. Afr. J. Microbiol. Res. 7, 3165–3170 (2013)

    Google Scholar 

  8. 8.

    Strohl, W.R.: Antimicrobials. In: Bull, A.T. (ed.) Microbial Diversity and Bioprocessing, pp. 336–355. American Society for Microbiology, Washington, D.C. (2004)

    Google Scholar 

  9. 9.

    Berdy, J.: Bioactive microbial metabolites. J. Antibiot. 58, 1–26 (2005)

    Google Scholar 

  10. 10.

    Prabavathy, V.R., Mathivanan, N., Murugesan, K.: Control of blast and sheath blight diseases of rice using antifungal metabolites produced by Streptomyces sp. PM5. Biol. Control 39, 313–319 (2006)

    Google Scholar 

  11. 11.

    Li, Q., Jiang, Y., Ning, P., Zheng, L., Huang, J., Li, G., Jiang, D., Hsiang, T.: Suppression of Magnaporthe oryzae by culture filtrates of Streptomyces globisporusJK-1. Biol. Control 58, 139–148 (2011)

    Google Scholar 

  12. 12.

    Shakeel, Q., Lyu, A., Zhang, J., Wu, M., Chen, S., Chen, W., Li, G., Yang, L.: Optimization of the cultural medium and conditions for production of antifungal substances by Streptomyces platensis 3–10 and evaluation of its efficacy in suppression of clubroot disease (Plasmodiophora brassicae) of oilseed rape. Biol. Control 101, 59–68 (2016)

    Google Scholar 

  13. 13.

    Boukaew, S., Prasertsan, P., Troulet, C., Bardin, M.: Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp. Biocontrol 62, 793–803 (2017)

    Google Scholar 

  14. 14.

    Sangkanu, S., Rukachaisirikul, V., Suriyachadkun, C., Phongpaichit, S.: Evaluation of antibacterial potential of mangrove sediment-derived actinomycetes. Microb. Pathog. 112, 303–312 (2017)

    Google Scholar 

  15. 15.

    Boukaew, S., Chuenchit, S., Petcharat, V.: Evaluation of Streptomyces spp. for biological control of Sclerotium root and stem rot and Ralstonia wilt of chili. Biocontrol 56, 365–374 (2011)

    Google Scholar 

  16. 16.

    Boukaew, S., Klinmanee, C., Prasertsan, P.: Potential for the integration of biological and chemical control of sheath blight disease caused by Rhizoctonia solani on rice. World J. Microbiol. Biotechnol. 29, 1885–1893 (2013)

    Google Scholar 

  17. 17.

    Boukaew, S., Prasertsan, P.: Suppression of rice sheath blight disease using heat stable culture filtrate of Streptomyces philanthi RM-1-138. Crop Prot. 61, 1–10 (2014)

    Google Scholar 

  18. 18.

    Zacky, F.A., Ting, A.S.Y.: Investigating the bioactivity of cells and cell-free extracts of Streptomyces griseus towards Fusarium oxysporum f. sp. cubense race 4. Biol. Control 66, 204–208 (2013)

    Google Scholar 

  19. 19.

    Chen, Y.Y., Chen, P.C., Tsay, T.T.: The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsici. Biol. Control 98, 34–42 (2016)

    Google Scholar 

  20. 20.

    Awla, H.K., Kadir, J., Othman, R., Rashid, T.S., Hamid, S., Wong, M.Y.: Plant growth-promoting abilities and biocontrol efficacy of Streptomyces sp. UPMRS4 against Pyricularia oryzae. Biol. Control 112, 55–63 (2017)

    Google Scholar 

  21. 21.

    Singh, S.P., Gaur, R.: Endophytic Streptomyces spp. underscore induction of defense regulatory genes and confers resistance against Sclerotium rolfsii in chickpea. Biol. Control 104, 44–56 (2017)

    Google Scholar 

  22. 22.

    Zain, M.E.: Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc. 15, 129–144 (2011)

    Google Scholar 

  23. 23.

    Gong, Y., Hounsa, A., Egal, S., Turner, P.C., Sutcliffe, A.E., Hall, A.J., Cardwell, K., Wild, C.P.: Postweaning exposure to aflatoxin results in impaired child growth: a longitudinal study in Benin, West Africa. Environ. Health Perspect. 112, 1334–1338 (2004)

    Google Scholar 

  24. 24.

    AOAC.: Official Methods of Analysis of the Association of Official Chemists. 14th ed. The Association of Official Analytical Chemists. Washington, D.C. (1984)

    Google Scholar 

  25. 25.

    Singh, R., Pradhan, K.: Determination of nitrogen and protein by Kjeldahl method. In: Forage Evaluation Science, p. 23, Pvt. Publishers Ltd., New Delhi (1981)

    Google Scholar 

  26. 26.

    Murphy, J., Riley, J.P.: A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962)

    Google Scholar 

  27. 27.

    Islam, M.R., Jeong, Y.T., Ryu, Y.J., Song, C.H., Lee, S.Y.: Identification and optimal culture condition of Streptomyces albidoflavus C247 producing antifungal agents against Rhizoctonia solani AG2-2. Mycobiology 27, 114–120 (2009)

    Google Scholar 

  28. 28.

    Vergopoulou, S., Galanopoulu, D., Markaki, P.: Methyl jasmonate stimulates aflatoxin B1 biosynthesis by Aspergillus parasiticus. J. Agric. Food Chem. 49, 3494–3498 (2001)

    Google Scholar 

  29. 29.

    Nogueira, J.H.C., Gonçalez, E., Galleti, S.R., Facanali, R., Marques, M.O.M., Felício, J.D.: Ageratum conyzoides essential oil as aflatoxin suppressor of Aspergillus flavus. Int. J. Food Microbiol. 137, 55–60 (2010)

    Google Scholar 

  30. 30.

    Komala, V.V., Ratnavathi, C.V., Kumar, B.V., Das, I.K.: Inhibition of aflatoxin B1 production by an antifungal component, eugenol in stored sorghum grains. Food Control 26, 139–146 (2012)

    Google Scholar 

  31. 31.

    Rammanee, K., Hongpattarakere, T.: Effects of tropical citrus essential oils on growth, aflatoxin production, and ultrastructure alterations of Aspergillus flavus and Aspergillus parasiticus. Food Bioprocess Technol. 4, 1050–1059 (2011)

    Google Scholar 

  32. 32.

    Sangmanee, P., Hongpattarakere, T.: Inhibitory of multiple antifungal components produced by Lactobacillus plantarum K35 on growth, aflatoxin production and ultrastructure alterations of Aspergillus flavus and Aspergillusparasiticus. Food Control 40, 224–233 (2014)

    Google Scholar 

  33. 33.

    Li, W.R., Shi, Q.S., Ouyang, Y.S., Chen, Y.B., Duan, S.S.: Antifungal effects of citronella oil against Aspergillus niger ATCC 16404. Appl. Microbiol. Biotechnol. 97, 7483–7492 (2013)

    Google Scholar 

  34. 34.

    Prapagdee, B., Kuekulvong, C., Mongkolsuk, S.: Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int. J. Biol. Sci. 4, 330–337 (2008)

    Google Scholar 

  35. 35.

    Leelasuphakul, W., Sivanunsakul, P., Phongpaichit, S.: Purification, characterization and synergistic activity of β-1, 3-glucanase and antibiotic extract from an antagonistic Bacillus subtilis NSRS 89 – 24 against rice blast and sheath blight. Enzym. Microb. Technol. 38, 990–997 (2006)

    Google Scholar 

  36. 36.

    Arrebola, E., Sivakumar, D., Korsten, L.: Effect of volatile compounds produced by Bacillus strains on postharvest decay in citrus. Biol. Control 53, 122–128 (2010)

    Google Scholar 

  37. 37.

    Li, Q., Ning, P., Zheng, L., Huang, J., Li, G., Hsiang, T.: Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol. Technol. 58, 157–165 (2010)

    Google Scholar 

  38. 38.

    Corcuff, R., Mercier, J., Tweddell, R., Arul, J.: Effect of water activity on the production of volatile organic compounds by Muscodor albus and their effect on three pathogens in stored potato. Fungal Biol. 115, 220–227 (2011)

    Google Scholar 

  39. 39.

    Kanjan, P., Hongpattarakere, T.: Antibacterial metabolites secreted under glucose-limited environment of themimicked proximal colon model by lactobacilli abundant in infant feces. Appl. Microbiol. Biotechnol. 100, 7651–7664 (2016)

    Google Scholar 

  40. 40.

    Niku-Paavola, M.L., Laitila, L., Mattila-Sandholm, T., Haikara, A.: New types of antimicrobial compounds produced by Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 86, 29–35 (1999)

    Google Scholar 

  41. 41.

    Ouhdouch, Y., Barakate, M., Finanse, C.: Actinomycetes of Moroccan habitats: isolation and screening for antifungal activities. Eur. J. Soil Biol. 37, 69–74 (2001)

    Google Scholar 

  42. 42.

    Tian, J., Zeng, X., Feng, Z., Miao, X., Peng, X., Wang, Y.: Zanthoxylum molle Rehd. essential oil as a potential natural preservative in management of Aspergillus flavus. Ind. Crops Prod. 60, 151–159 (2014)

    Google Scholar 

  43. 43.

    Tian, J., Huang, B., Luo, X., Zeng, H., Ban, X., He, J., Wang, Y.: The control of Aspergillus flavus with Cinnamomum jensenianum Hand.-Mazz essential oil and its potential use as a food preservative. Food Chem. 130, 520–527 (2012)

    Google Scholar 

  44. 44.

    Joshi, S., Bharucha, C., Jha, S., Yadav, S., Nerurkar, A., Desai, A.J.: Biosurfactant production using molasses and whey under thermophilic conditions. Bioresour. Technol. 99, 195–199 (2008)

    Google Scholar 

  45. 45.

    Rashedi, H., Assadi, M.M., Jamshidi, E., Bonakdarpour, B.: Production of rhamnolipids by Pseudomonas aeruginosa growing on carbon sources. Int. J. Environ. Sci. Technol. 3, 297–303 (2006)

    Google Scholar 

  46. 46.

    Srinivasan, M.C., Laxman, R.S., Deshpande, M.V.: Physiology and nutritional aspects of actinomycetes: an overview. World J. Microbiol. Biotechnol. 7, 171–184 (1991)

    Google Scholar 

  47. 47.

    Sole, M., Francia, A., Rius, N., Loren, J.G.: The role of pH in the glucose effect on prodigiosin production by non-proliferating cells of Serratia marcescens. Lett. Appl. Microbiol. 25, 81–84 (1997)

    Google Scholar 

  48. 48.

    Boukaew, S., Prasertsan, P.: Factors affecting antifungal activity of Streptomyces philanthi RM-1-138 against Rhizoctonia solani. World J. Microbiol. Biotechnol. 30, 323–329 (2014)

    Google Scholar 

  49. 49.

    Battacharyya, B.K., Pal, S.C., Sen, S.K.: Antibiotic production by Streptomyces hygroscopicus D1.5: cultural effect. Rev. Microbiol. 29, 49–52 (1998)

    Google Scholar 

  50. 50.

    Yi, Y.J., Li, Y.S., Xia, B., Li, W.P., Pang, L., Tong, Z.D.: Optimization of medium composition and culture conditions for antifungal activity of a tomato endophytic bacterium. Biol. Control 82, 69–75 (2014)

    Google Scholar 

Download references

Acknowledgements

This research study was financially supported by the Agricultural Research Development Agency (Public Organization) (PRP5905021490) and Thailand Research Fund (RTA6080010).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sawai Boukaew.

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

Boukaew, S., Petlamul, W. & Prasertsan, P. Tuna Condensate Waste with Molasses as a Renewable Substrate for Antifungal Compounds by Streptomyces philanthi RL-1-178 Against Aflatoxingenic B1 (AFB1) Aspergillus flavus. Waste Biomass Valor 11, 1321–1331 (2020). https://doi.org/10.1007/s12649-018-0530-4

Download citation

Keywords

  • A. flavus
  • Antifungal activity
  • Molasses
  • S. philanthi
  • Tuna condensate
  • Waste utilization