Skip to main content
Log in

Induced Biofilm Cultivation Enhances Riboflavin Production by an Intertidally Derived Candida famata

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The aim of the investigation was to ascertain if surface attachment of Candida famata and aeration enhanced riboflavin production. A newly designed polymethylmethacrylate (PMMA) conico-cylindrical flask (CCF) holding eight equidistantly spaced rectangular strips mounted radially on a circular disk allowed comparison of riboflavin production between CCFs with hydrophobic surface (PMMA-CCF), hydrophilic glass surface (GS-CCF), and 500-ml Erlenmeyer flask (EF). Riboflavin production (mg/l) increased from 12.79 to 289.96, from 54.44 to 238.14, and from 36.98 to 158.71 in the GS-CCF, EF, and PMMA-CCF, respectively, when C. famata was grown as biofilm-induced cultures in contrast to traditional planktonic culture. Production was correlated with biofilm formation and planktonic growth was suppressed in cultivations that allowed higher biofilm formation. Enhanced aeration increased riboflavin production in hydrophilic vessels. Temporal pattern of biofilm progression based on two-channel fluorescence detection of extracellular polymeric substances and whole cells in a confocal laser scanning microscope followed by application of PHLIP and ImageJ volume viewer software demonstrated early maturity of a well-developed, stable biofilm on glass in contrast to PMMA surface. A strong correlation between hydrophilic reactor surface, aeration, biofilm formation, and riboflavin production was established in C. famata. Biofilm culture is a new-found means to improve riboflavin production by C. famata.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Ortega-Morales, B. O., Chan-Bacab, M. J., De la Rosa-García, S. D. C., & Camacho-Chab, J. C. (2010). Valuable processes and products from marine intertidal microbial communities. Current Opinion in Biotechnology, 21(3), 346–352.

    Article  CAS  Google Scholar 

  2. Decho, A. W. (2000). Microbial biofilms in intertidal systems: An overview. Continental Shelf Research, 20(10–11), 1257–1273.

    Article  Google Scholar 

  3. Penesyan, A., Kjelleberg, S., & Egan, S. (2010). Development of novel drugs from marine surface associated microorganisms. Marine Drugs, 8(3), 438–459.

    Article  CAS  Google Scholar 

  4. Stahmann, K.-P., Revuelta, J. L., & Seulberger, H. (2000). Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Applied Microbiology and Biotechnology, 53(5), 509–516.

    Article  CAS  Google Scholar 

  5. Ramage, G., Rajendran, R., Gutierrez-Correa, M., Jones, B., & Williams, C. (2011). Aspergillus biofilms: Clinical and industrial significance. FEMS Microbiology Letters, 324(2), 89–97.

    Article  CAS  Google Scholar 

  6. Sarkar, S., Roy, D., & Mukherjee, J. (2011). Enhanced protease production in a polymethylmethacrylate conico-cylindrical flask by two biofilm-forming bacteria. Bioresource Technology, 102(2), 1849–1855.

    Article  CAS  Google Scholar 

  7. Mitra, S., Sarkar, S., Gachhui, R., & Mukherjee, J. (2011). A novel conico-cylindrical flask aids easy identification of critical process parameters for cultivation of marine bacteria. Applied Microbiology and Biotechnology, 90(1), 321–330.

    Article  CAS  Google Scholar 

  8. Mitra, S., Banerjee, P., Gachhui, R., & Mukherjee, J. (2011). Cellulase and xylanase activity in relation to biofilm formation by two intertidal filamentous fungi in a novel polymethylmethacrylate conico-cylindrical flask. Bioprocess and Biosystems Engineering, 34(9), 1087–1101.

    Article  CAS  Google Scholar 

  9. Hagler, A. N., & Mendonca-Hagler, L. C. (1981). Yeasts from marine and estuarine waters with different levels of pollution in the state of Rio de Janeiro, Brazil. Applied and Environmental Microbiology, 41(1), 173–178.

    CAS  Google Scholar 

  10. Yatsyshyn, V. Y., Fedorovych, D. V., & Sibirny, A. A. (2010). Medium optimization for production of flavin mononucleotide by the recombinant strain of the yeast Candida famata using statistical designs. Biochemical Engineering Journal, 49(1), 52–60.

    Article  CAS  Google Scholar 

  11. Kalingan, A. E., & Liao, C.-M. (2002). Influence of type and concentration of flavinogenic factors on production of riboflavin by Eremothecium ashbyii NRRL 1363. Bioresource Technology, 82(3), 219–224.

    Article  CAS  Google Scholar 

  12. Villena, G. K., & Gutiérrez-Correa, M. (2006). Production of cellulase by Aspergillus niger biofilms developed on polyester cloth. Letters in Applied Microbiology, 43(3), 262–268.

    Article  CAS  Google Scholar 

  13. Villena, G. K., & Gutiérrez-Correa, M. (2007). Morphological patterns of Aspergillus niger biofilms and pellets related to lignocellulolytic enzyme productivities. Letters in Applied Microbiology, 45(3), 231–237.

    Article  CAS  Google Scholar 

  14. Paramonova, E., Krom, B. P., van der Mei, H. C., Busscher, H. J., & Sharma, P. K. (2009). Hyphal content determines the compression strength of Candida albicans biofilms. Microbiology, 155(6), 1997–2003.

    Article  CAS  Google Scholar 

  15. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350–356.

    Article  CAS  Google Scholar 

  16. Raunkjær, K., Hvitved-Jacobsen, T., & Nielsen, P. H. (1994). Measurement of pools of protein, carbohydrate and lipid in domestic wastewater. Water Research, 28(2), 251–262.

    Article  Google Scholar 

  17. Chrzanowski, Ł., Kaczorek, E., & Olszanowski, A. (2005). Relation between Candida maltosa hydrophobicity and hydrocarbon biodegradation. World Journal of Microbiology and Biotechnology, 21(6–7), 1273–1277.

    Article  CAS  Google Scholar 

  18. Mueller, L. N., De Brouwer, J. F. C., Almeida, J. S., Stal, L. J., & Xavier, J. B. (2006). Analysis of a marine phototrophic biofilm by confocal laser scanning microscopy using the new image quantification software PHLIP. BMC Ecology, 6(1), 1–15.

    Article  Google Scholar 

  19. Eshed, L., Yaron, S., & Dosoretz, C. G. (2008). Effect of permeate drag force on the development of a biofouling layer in a pressure-driven membrane separation system. Applied and Environmental Microbiology, 74(23), 7338–7347.

    Article  CAS  Google Scholar 

  20. Chandra, J., Patel, J. D., Li, J., Zhou, G., Mukherjee, P. K., McCormick, T. S., et al. (2005). Modification of surface properties of biomaterials influences the ability of Candida albicans to form biofilms. Applied and Environmental Microbiology, 71(12), 8795–8801.

    Article  CAS  Google Scholar 

  21. Martinez, L. R., & Casadevall, A. (2007). Cryptococcus neoformans biofilm formation depends on surface support and carbon source and reduces fungal cell susceptibility to heat, cold, and UV Light. Applied and Environmental Microbiology, 73(14), 4592–4601.

    Article  CAS  Google Scholar 

  22. Ryan, B. J., & Poduska, K. M. (2008). Roughness effects on contact angle measurements. American Journal of Physics, 76(11), 1074–1077.

    Article  CAS  Google Scholar 

  23. Heydorn, A., Nielsen, A. T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B. K., et al. (2000). Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology, 146(10), 2395–2407.

    CAS  Google Scholar 

  24. Da Silva, W. J., Seneviratne, J., Samaranayake, L. P., & Del Bel Cury, A. A. (2010). Bioactivity and architecture of Candida albicans biofilms developed on poly (methyl methacrylate) resin surface. Journal of Biomedical Materials Research. Part B, Applied Biomaterials, 94(1), 149–156.

    Google Scholar 

  25. Malm, A., Chudzik, B., Piersiak, T., & Gawron, A. (2010). Glass surface as potential in vitro substratum for Candida famata biofilm. Annals of Agricultural and Environmental Medicine, 17(1), 115–118.

    Google Scholar 

  26. Villena, G. K., Fujikawa, T., Tsuyumu, S., & Gutiérrez-Correa, M. (2010). Structural analysis of biofilms and pellets of Aspergillus niger by confocal laser scanning microscopy and cryo scanning electron microscopy. Bioresource Technology, 101(6), 1920–1926.

    Article  CAS  Google Scholar 

  27. Qureshi, N., Annous, B. A., Ezeji, T. C., Karcher, P., & Maddox, I. S. (2005). Biofilm reactors for industrial bioconversion process: Employing potential of enhanced reaction rates. Microbial Cell Factories, 4(24), 1–21.

    Google Scholar 

  28. Cao, N., Du, J., Chen, C., Gong, C. S., & Tsao, G. T. (1997). Production of fumaric acid by immobilized Rhizopus using rotary biofilm contactor. Applied Biochemistry and Biotechnology, 63–65(1–3), 387–394.

    Article  Google Scholar 

  29. Dmytruk, K. V., Yatsyshyn, V. Y., Sybirna, N. O., Fedorovych, D. V., & Sibirny, A. A. (2011). Metabolic engineering and classic selection of the yeast Candida famata (Candida flareri) for construction of strains with enhanced riboflavin production. Metabolic Engineering, 13(1), 82–88.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support to JM, RG (DBT sanction no. BT/PR11479/AAQ/03/423/2008), and DST-PURSE, 2009–2010 is thankfully acknowledged. The authors wish to thank Dr. Arun Bandyopadhyay and Mrs. Banasri Das for their help during confocal microscopy. DT wishes to thank the authorities of IIT (Guwahati) for the summer internship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joydeep Mukherjee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Estimated 3D surface plots of C. famata biofilm following analysis by ImageJ using the interactive 3D surface plot plugin 2.32 after A 1, B 2, C 3, and D 4 days on glass surface and after E 4, F 5, G 6, and H 7 days on the PMMA surface. Color only in online version (JPEG 30 kb)

High resolution image file (TIFF 2572 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mitra, S., Thawrani, D., Banerjee, P. et al. Induced Biofilm Cultivation Enhances Riboflavin Production by an Intertidally Derived Candida famata . Appl Biochem Biotechnol 166, 1991–2006 (2012). https://doi.org/10.1007/s12010-012-9626-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-012-9626-7

Keywords

Navigation