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Catalysis Letters

, Volume 148, Issue 2, pp 712–724 | Cite as

A Statistical Approach to Optimize Cold Active β-Galactosidase Production by an Arctic Sediment Pscychrotrophic Bacteria, Enterobacter ludwigii (MCC 3423) in Cheese Whey

  • Aneesa P. Alikunju
  • Susan Joy
  • Mujeeb Rahiman
  • Emilda Rosmine
  • Ally C. Antony
  • Solly Solomon
  • K. Manjusha
  • A. V. Saramma
  • K. P. Krishnan
  • A. A. Mohamed Hatha
Article

Abstract

Cold active β-galactosidases which catalyze lactose hydrolysis and transglycosylation reactions at low temperature make them highly potential biocatalyst in biotechnology, pharmaceutical and food processing industries. Moreover, an interest towards the utilization of diary industrial waste, whey and its constituents, for manufacturing a wide range of valuable products at reliable cost is increasing among researchers in order to facilitate its wider commercial use. In the present study, the fermentation parameters for the maximum production of cold active β-galactosidase from a psychrotrophic bacterium, Enterobacter ludwigii in cheese whey was optimized by exploring statistical methods, Plackett-Burman design (PBD) and central composite design (CCD). Three most significant factors viz, pH, whey and tryptone out of 11 were selected by PBD and were further optimized by response surface methodology using CCD. The optimal levels of pH, whey and tryptone were indicated as 7.3, 82 (v/v) % and 3.84 g% respectively. An overall 3.6-fold increase in cold active β-galactosidase production (34.37 U/mL) was achieved in optimized medium compared to the yield from unoptimized medium. The quadratic regression model was proven to be adequate (p = 0.0001, R 2  = 0.9880, CV = 7.96%) and the response (cold active β-galactosidase production) obtained on validation coincident with the predicted value.

Graphical Abstract

Keywords

Arctic Cold active β-galactosidase Response surface methodology Whey 

Notes

Acknowledgements

The authors are thankful to UGC-BSR, India for funding the research work (UGC Grant No. F.No. 25-1/2014-15(BSR)/5-24/2007/(BSR). Authors are also thankful to the Department of Marine Biology, Microbiology and Biochemistry and Sophisticated Testing and Instrumentation Centre (STIC) at Cochin University of Science and Technology (CUSAT) and National Centre for Antarctic and Ocean Research (NCAOR) for providing the facilities to carry out the research. Authors acknowledge Dr. C. K. Radhakrishnan and K. T. Thomas for their valuable suggestions and support.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest in the publication.

References

  1. 1.
    Wierzbicka-Woś A, Cieśliński H, Wanarska M et al (2011) A novel cold-active β-d-galactosidase from the Paracoccus sp. 32d - gene cloning, purification and characterization. Microb Cell Fact 10:108–120CrossRefGoogle Scholar
  2. 2.
    Harju M, Kallioinen H, Tossavainen O (2012) Lactose hydrolysis and other conversions in dairy products: technological aspects. Int Dairy J 22(2):104–109CrossRefGoogle Scholar
  3. 3.
    Pawlak-Szukalska A, Wanarska M, Popinigis AT et al (2014) A novel cold-active β-d-galactosidase with transglycosylation activity from the Antarctic Arthrobacter sp. 32cB—gene cloning, purification and characterization. Process Biochem 49(12):2122–2133CrossRefGoogle Scholar
  4. 4.
    Hoyoux A, Jennes I, Dubois P et al (2001) Cold-adapted β-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis.Appl Environ Microbiol 67(4):1529–1535CrossRefGoogle Scholar
  5. 5.
    Fernandes S, Geueke B, Delgado O et al (2002) β-Galactosidase from a cold-adapted bacterium: purification, characterization and application for lactose hydrolysis. Appl Microbiol Biotechnol 58:313–321CrossRefGoogle Scholar
  6. 6.
    Nakagawa T, Fujimoto Y, Ikehata R et al (2006) Purification and molecular characterization of cold-active β-galactosidase from Arthrobacter psychrolactophilus strain F2. Appl Microbiol Biotechnol 72:720–725CrossRefGoogle Scholar
  7. 7.
    Rastall RA, Maitin V (2002) Prebiotics and synbiotics: towards the next generation. Curr Opin Biotechnol 13(5):490–496CrossRefGoogle Scholar
  8. 8.
    Splechtna B, Nguyen TH, Steinbock M et al (2006) Production of prebiotic galacto-oligosaccharides from lactose using β-galactosidases from Lactobacillus reuteri.J Agric Food Chem 54(14):4999–5006CrossRefGoogle Scholar
  9. 9.
    Białkowska AM, Cieśliński H, Nowakowska KM et al (2009) A new β-galactosidase with a low temperature optimum isolated from the Antarctic Arthrobacter sp. 20B: gene cloning, purification and characterization. Arch Microbiol 191:825–835CrossRefGoogle Scholar
  10. 10.
    Schmidt M, Stougaard P (2010) Identification, cloning and expression of a cold-active β-galactosidase from a novel Arctic bacterium, Alkalilactibacillus ikkense. Environ Technol 31:1107–1114CrossRefGoogle Scholar
  11. 11.
    Alikkunju AP, Sainjan N, Silvester R et al (2016) Screening and characterization of cold-active β-galactosidase producing psychrotrophic Enterobacter ludwigii from the sediments of Arctic Fjord. Appl Biochem Biotechnol 180(3):477–490CrossRefGoogle Scholar
  12. 12.
    Siso MIG (1996) The biotechnological utilization of cheese whey: a review. Bioresour Technol 57:1–11CrossRefGoogle Scholar
  13. 13.
    Smithers GW (2008) Whey and whey proteins—from gutter to gold. Int Diary J 18:695–704CrossRefGoogle Scholar
  14. 14.
    Illanes A (2011) Whey upgrading by enzyme biocatalysis. Electron J Biotechnol 14:1–28CrossRefGoogle Scholar
  15. 15.
    Das P, Mukherjee S, Sen R (2009) Substrate dependent production of extracellular biosurfactant by a marine bacterium. Bioresour Technol 100:1015–1019CrossRefGoogle Scholar
  16. 16.
    Venetsaneas N, Antonopoulou G, Stamatelatou K et al (2009) Using cheese whey for hydrogen and methane generation in a two-stage continuous process with alternative pH controlling approaches. Bioresour Technol 100(15):3713–3717CrossRefGoogle Scholar
  17. 17.
    Geiger B, Nguyen H, Wenig S et al (2016) From by-product to valuable components : efficient enzymatic conversion of lactose in whey using β-galactosidase from Streptococcus thermophilus. Biochem Eng J 116:45–53CrossRefGoogle Scholar
  18. 18.
    Gao H, Liu M, Liu J et al (2009) Medium optimization for the production of avermectin B1a by Streptomyces avermitilis 14-12A using response surface methodology. Bioresour Technol 100(17):4012–4016CrossRefGoogle Scholar
  19. 19.
    Xiong Y, Liu J, Song H et al (2004) Enhanced production of extracellular ribonuclease from Aspergillus niger by optimization of culture conditions using response surface methodology. Biochem Eng J 21:27–32CrossRefGoogle Scholar
  20. 20.
    Deepak V, Kalishwaralal K, Ramkumarpandian S et al (2008) Optimization of media composition for Nattokinase production by Bacillus subtilis using response surface methodology. Bioresour Technol 99:8170–8174CrossRefGoogle Scholar
  21. 21.
    Singh V, Haque S, Niwas R et al (2017) Strategies for fermentation medium optimization: an in-depth review. Front Microbiol.  https://doi.org/10.3389/fmicb.2016.02087 Google Scholar
  22. 22.
    Keskin Gundogdu T, Deniz I, Caliskan G et al (2016) Experimental design methods for bioengineering applications. Crit Rev Biotechnol 36:368–388CrossRefGoogle Scholar
  23. 23.
    Elibol M (2004) Optimization of medium composition for actinorhodin production by Streptomyces coelicolor A3 (2) with response surface methodology. Process Biochem 39:1057–1062CrossRefGoogle Scholar
  24. 24.
    Basha M, Rajasimman M (2015) Fermentative production and optimization of mevastatin in submerged fermentation using Aspergillus terreus. Biotechnol Rep 6:124–128CrossRefGoogle Scholar
  25. 25.
    Almeida DG, Soares da Silva RCF, Luna JM et al (2017) Response surface methodology for optimizing the production of biosurfactant by Candida tropicalis on industrial waste substrates. Front Microbiol 8(157):1–13Google Scholar
  26. 26.
    Liu J, Xing J, Chang T et al (2005) Optimization of nutritional conditions for nattokinase production by Bacillus natto NLSSE using statistical experimental methods. Process Biochem 40:2757–2762CrossRefGoogle Scholar
  27. 27.
    Thys RCS, Guzzon SO, Cladera-olivera F et al (2006) Optimization of protease production by Microbacterium sp. in feather meal using response surface methodology. Process Biochem 41:67–73CrossRefGoogle Scholar
  28. 28.
    Patil MD, Shinde KD, Patel G et al (2016) Use of response surface method for maximizing the production of arginine deiminase by Pseudomonas putida. Biotechnol Rep 10:29–37CrossRefGoogle Scholar
  29. 29.
    Rosmine E, Sainjan NC, Silvester R et al (2017) Statistical optimisation of xylanase production by estuarine Streptomyces sp. and its application in clarification of fruit juice. J Genet Eng Biotechnol.  https://doi.org/10.1016/j.jgeb.2017.06.001 Google Scholar
  30. 30.
    Hussain F, Kamal S, Rehman S et al (2017) Alkaline protease production using response surface methodology, characterization and industrial exploitation of alkaline protease of Bacillus substilis sp. Catal Lett 147(5):1204–1213CrossRefGoogle Scholar
  31. 31.
    AOAC (2006) Official methods of analysis. The association of official analytical chemists, 18th edn. AOAC, ArlingtonGoogle Scholar
  32. 32.
    Pearson D (1976) Chemical analysis of foods, 7th edn. Church Hill Livingstone, LondonGoogle Scholar
  33. 33.
    Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226(1):497–509Google Scholar
  34. 34.
    Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor, New York, pp. 352–355Google Scholar
  35. 35.
    Cruz R, Cruz VDA, Belot JG et al (1999) Production of transgalactosylated oligosaccharides (TOS) by galactosyltransferase activity from Penicillium simplicissimum. Bioresour Technol 70:165–171CrossRefGoogle Scholar
  36. 36.
    Zadow JG (1994) Utilization of milk components: whey. In: Robinson RK (ed) Modern dairy technology, advances in milk processing, vol 1, 2nd edn. Springer, Boston, p 504Google Scholar
  37. 37.
    Khan H, Flint SH, Yu P (2013) Development of a chemically defined medium for the production of enterolysin A from Enterococcus faecalis. J Appl Microbiol 114:1092–1102CrossRefGoogle Scholar
  38. 38.
    Dalev PG (1994) Utilization of waste whey as a protein source for production of iron proteinate: an antianemic preparation. Bioresour Technol 48:75–77CrossRefGoogle Scholar
  39. 39.
    Mawson AJ (1994) Bioconversions for whey utilization and waste abatement. Bioresour Technol 47(3):195–203CrossRefGoogle Scholar
  40. 40.
    Saddoud A, Hassaı I, Sayadi S (2007) Anaerobic membrane reactor with phase separation for the treatment of cheese whey. Bioresour Technol 98:2102–2108CrossRefGoogle Scholar
  41. 41.
    Daverey A, Pakshirajan K (2009) Production, characterization and properties of sophorolipids from the Yeast Candida bombicola using a low-cost fermentative medium. Appl Biochem Biotechnol 158:663–674CrossRefGoogle Scholar
  42. 42.
    Raganati F, Olivieri G, Procentese A, Russo ME, Salatino P, Marzocchella A (2013) Butanol production by bioconversion of cheese whey in a continuous packed bed reactor. Bioresour Technol 138:259–265CrossRefGoogle Scholar
  43. 43.
    Ghosh M, Pulicherla KK, Rekha VPB et al (2013) Optimisation of process conditions for lactose hydrolysis in paneer whey with cold-active β-galactosidase from psychrophilic Thalassospira frigidphilosprofundus. Int J Dairy Technol 66(2):256–263CrossRefGoogle Scholar
  44. 44.
    Bansal S, Oberoi HS, Dhillon GS et al (2008) Production of β-galactosidase by Kluyveromyces marxianus MTCC 1388 using whey and effect of four different methods of enzyme extraction on β-galactosidase activity. Indian J Microbiol 48:337–341CrossRefGoogle Scholar
  45. 45.
    Siso MIG (1994) β-Galactosidase production by Kluyveromyces lactis on milk whey: batch versus fed-batch cultures. Process Biochem 29:565–568CrossRefGoogle Scholar
  46. 46.
    Raol GG, Raol BV, Prajapati VS et al (2015) Utilization of agro-industrial waste for β-galactosidase production under solid state fermentation using halotolerant Aspergillus tubingensis GR1 isolate. 3 Biotech 5:411–421CrossRefGoogle Scholar
  47. 47.
    Myers RH, Montogomery DC (2002) Response surface methodology: process and product optimization using designed experiments, 2nd edn. Wiley, New YorkGoogle Scholar
  48. 48.
    Muralidhar RV, Chirumamila RR, Marchant R et al (2001) A response surface approach for the comparison of lipase production by Candida cylindracea using two different carbon sources. Biochem Eng J 9:17–23CrossRefGoogle Scholar
  49. 49.
    Garg G, Mahajan R, Kaur A et al (2011) Xylanase production using agro-residue in solidstate fermentation from Bacillus pumilus ASH for bio-delignification of wheat straw pulp. Biodegradation 22:1143–1154CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Aneesa P. Alikunju
    • 1
  • Susan Joy
    • 1
  • Mujeeb Rahiman
    • 2
  • Emilda Rosmine
    • 1
  • Ally C. Antony
    • 1
  • Solly Solomon
    • 1
  • K. Manjusha
    • 3
  • A. V. Saramma
    • 1
  • K. P. Krishnan
    • 4
  • A. A. Mohamed Hatha
    • 1
  1. 1.Department of Marine Biology, Microbiology and BiochemistryCochin University of Science and TechnologyCochinIndia
  2. 2.Department of Aquaculture and Fishery MicrobiologyMES Ponnani CollegePonnaniIndia
  3. 3.Department of MicrobiologySt.Xaviers College for WomenAluvaIndia
  4. 4.National Center for Antarctic and Ocean ResearchGoaIndia

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