Article Search
닫기

Microbiology and Biotechnology Letters

보문(Article)

View PDF

Bioactive Compounds / Food Microbiology  |  Biomolecules

Microbiol. Biotechnol. Lett. 2020; 48(1): 12-23

https://doi.org/10.4014/mbl.1909.09016

Received: October 1, 2019; Accepted: November 25, 2019

Enhancement of β-Cyclodextrin Production and Fabrication of Edible Antimicrobial Films Incorporated with Clove Essential Oil/β-cyclodextrin Inclusion Complex

Mohamed Farahat *

Botany and Microbiology Department, Faculty of Science, Cairo University, 12613 Giza, Egypt

Edible films containing antimicrobial agents can be used as safe alternatives to preserve food products. Essential oils are well-recognized antimicrobials. However, their low water solubility, volatility and high sensitivity to oxygen and light limit their application in food preservation. These limitations could be overcome by embedding these essential oils in complexed product matrices exploiting the encapsulation efficiency of β-cyclodextrin. This study focused on the maximization of β-cyclodextrin production using cyclodextrin glucanotransferase (CGTase) and the evaluation of its encapsulation efficacy to fabricate edible antimicrobial films. Response surface methodology (RSM) was used to optimize CGTase production by Brevibacillus brevis AMI-2 isolated from mangrove sediments. This enzyme was partially purified using a starch adsorption method and entrapped in calcium alginate. Cyclodextrin produced by the immobilized enzyme was then confirmed using high performance thin layer chromatography, and its encapsulation efficiency was investigated. The clove oil/β-cyclodextrin inclusion complexes were prepared using the coprecipitation method, and incorporated into chitosan films, and subjected to antimicrobial testing. Results revealed that β-cyclodextrin was produced as a major product of the enzymatic reaction. In addition, the incorporation of clove oil/β-cyclodextrin inclusion complexes significantly increased the antimicrobial activity of chitosan films against Staphylococcus aureus, Staphylococcus epidermidis, Salmonella Typhimurium, Escherichia coli, and Candida albicans. In conclusion, B. brevis AMI-2 is a promising source for CGTase to synthesize β-cyclodextrin with considerable encapsulation efficiency. Further, the obtained results suggest that chitosan films containing clove oils encapsulated in β-cyclodextrin could serve as edible antimicrobial food-packaging materials to combat microbial contamination.

Keywords: &beta,-cyclodextrin glucanotransferase, Brevibacillus, RSM, optimization, immobilization

  1. Malhotra B, Keshwani A, Kharkwal H. 2015. Antimicrobial food packaging: potential and pitfalls. Front Microbiol. 6: 611.
    CrossRef
  2. Niu B, Shao P, Chen H, Sun P. 2019. Structural and physiochemical characterization of novel hydrophobic packaging films based on pullulan derivatives for fruits preservation. Carbohydr. Polym. 208: 276-284.
    Pubmed CrossRef
  3. Liu X, Han W, Zhu Y, Xuan H, Ren J, Zhang J, et al. 2018. Antioxidative and antibacterial self-healing edible polyelectrolyte multilayer film in fresh-cut fruits. J. Nanosci. Nanotechnol. 18: 2592-2600.
    Pubmed CrossRef
  4. Shaikh M, Haider S, Ali TM, Hasnain A. 2019. Physical, thermal, mechanical and barrier properties of pearl millet starch films as affected by levels of acetylation and hydroxypropylation. Int. J. Biol. Macromol. 124: 209-219.
    Pubmed CrossRef
  5. Pereira dos Santos E, Nicácio PHM, Coêlho Barbosa F, Nunes da Silva H, Andrade ALS, Lia Fook MV, et al. 2019. Chitosan/essential oils formulations for potential use as wound dressing: physical and antimicrobial properties. Materials (Basel) 12: 2223.
    Pubmed KoreaMed CrossRef
  6. Gao HX, He Z, Sun Q, He Q, Zeng WC. 2019. A functional polysaccharide film forming by pectin, chitosan, and tea polyphenols. Carbohydr. Polym. 215: 1-7.
    Pubmed CrossRef
  7. Zhong Y, Zhuang C, Gu W, Zhao Y. 2019. Effect of molecular weight on the properties of chitosan films prepared using electrostatic spraying technique. Carbohydr. Polym. 212: 197-205.
    Pubmed CrossRef
  8. Abanoz HS, Kunduhoglu B. 2018. Antimicrobial activity of a bacteriocin produced by Enterococcus faecalis KT11 against some Pathogens and antibiotic-eesistant bacteria. Korean J. Food Sci. Anim. Resour. 38: 1064-1079.
    Pubmed KoreaMed CrossRef
  9. Miceli de Farias F, dos Santos Nascimento J, Cabral da Silva Santos O, de Freire Bastos M do C. 2019. Study of the effectiveness of staphylococcins in biopreservation of Minas fresh (Frescal) cheese with a reduced sodium content. Int. J. Food Microbiol. 304: 19-31.
    Pubmed CrossRef
  10. Sun C, Li Y, Cao S, Wang H, Jiang C, Pang S, et al. 2018. Antibacterial activity and mechanism of action of bovine lactoferricin derivatives with symmetrical amino acid sequences. Int. J. Mol. Sci. 19: 2951.
    Pubmed KoreaMed CrossRef
  11. Silva F, Domingues FC. 2017. Antimicrobial activity of coriander oil and its effectiveness as food preservative. Crit. Rev. Food Sci. Nutr. 57: 35-47.
    Pubmed CrossRef
  12. Hu Q, Zhou M, Wei S. 2018. Progress on the antimicrobial activity research of clove oil and eugenol in the food antisepsis field. J. Food Sci. 83: 1476-1483.
    Pubmed CrossRef
  13. Elshafie HS, Gruľová D, Baranová B, Caputo L, De Martino L, Sedlák V, et al. 2019. Antimicrobial activity and chemical composition of essential oil extracted from Solidago canadensis L. growing wild in Slovakia. Molecules 24(7). pii: E1206.
    Pubmed KoreaMed CrossRef
  14. de Rostro-Alanis MJ, Báez-González J, Torres-Alvarez C, ParraSaldívar R, Rodriguez-Rodriguez J, Castillo S. 2019. Chemical composition and biological activities of oregano essential oil and its fractions obtained by vacuum distillation. Molecules 24(10). pii: E1904.
    Pubmed KoreaMed CrossRef
  15. Almeida ET da C, de Souza GT, de Sousa Guedes JP, Barbosa IM, de Sousa CP, Castellano LRC, et al. 2019. Mentha piperita L. essential oil inactivates spoilage yeasts in fruit juices through the perturbation of different physiological functions in yeast cells. Food Microbiol. 82: 20-29.
    Pubmed CrossRef
  16. Shi Y, Huang S, He Y, Wu J, Yang Y. 2018. Navel orange peel essential oil to control food spoilage molds in potato slices. J. Food Prot. 81: 1496-1502.
    Pubmed CrossRef
  17. Marchese A, Barbieri R, Coppo E, Orhan IE, Daglia M, Nabavi SF, et al. 2017. Antimicrobial activity of eugenol and essential oils containing eugenol: A mechanistic viewpoint. Crit. Rev. Microbiol. 43: 668-689.
    Pubmed CrossRef
  18. Zhang Y, Wang Y, Zhu X, Cao P, Wei S, Lu Y. 2017. Antibacterial and antibiofilm activities of eugenol from essential oil of Syzygium aromaticum (L.) Merr. & L. M. Perry (clove) leaf against periodontal pathogen Porphyromonas gingivalis. Microb. Pathog. 113: 396-402.
    Pubmed CrossRef
  19. Mohamed MSM, Abdallah AA, Mahran MH, Shalaby AM. 2018. Potential alternative treatment of ocular bacterial infections by oil derived from Syzygium aromaticum flower (Clove). Curr. Eye Res. 43: 873-881.
    Pubmed CrossRef
  20. Devi KP, Sakthivel R, Nisha SA, Suganthy N, Pandian SK. 2013. Eugenol alters the integrity of cell membrane and acts against the nosocomial pathogen Proteus mirabilis. Arch Pharm. Res. 36: 282-292.
    Pubmed CrossRef
  21. Devi KP, Nisha SA, Sakthivel R, Pandian SK. 2010. Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J. Ethnopharmacol. 130: 107-115.
    Pubmed CrossRef
  22. Xu J-G, Liu T, Hu Q-P, Cao X-M. 2016. Chemical composition, antibacterial properties and mechanism of action of essential oil from clove buds against Staphylococcus aureus. Molecules 21: 1194.
    Pubmed KoreaMed CrossRef
  23. Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L. 2009. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J. Med. Microbiol. 58: 1454-1462.
    Pubmed CrossRef
  24. Kfoury M, Auezova L, Greige-Gerges H, Fourmentin S. 2015. Promising applications of cyclodextrins in food: Improvement of essential oils retention, controlled release and antiradical activity. Carbohydr. Polym. 131: 264-272.
    Pubmed CrossRef
  25. Burt S. 2004. Essential oils: their antibacterial properties and potential applications in foods—a review. Int. J. Food Microbiol. 94: 223-253.
    Pubmed CrossRef
  26. Kotronia M, Kavetsou E, Loupassaki S, Kikionis S, Vouyiouka S, Detsi A. 2017. Encapsulation of Oregano (Origanum onites L.) essential oil in β-Cyclodextrin (β-CD): synthesis and characterization of the inclusion complexes. Bioengineering 4(3). pii: E74.
    Pubmed KoreaMed CrossRef
  27. Sun X, Sui S, Ference C, Zhang Y, Sun S, Zhou N, et al. 2014. Antimicrobial and mechanical properties of β-cyclodextrin inclusion with essential oils in chitosan films. J. Agric. Food Chem. 62: 8914-8918.
    Pubmed CrossRef
  28. Del Valle EMM. 2004. Cyclodextrins and their uses: A review. Process Biochem. 39: 1033-1046.
    CrossRef
  29. Qi Q, Zimmermann W. 2005. Cyclodextrin glucanotransferase:From gene to applications. Appl. Microbiol. Biotechnol. 66: 475-485.
    Pubmed CrossRef
  30. Zain WSWM, Illias RM, Salleh MM, Hassan O, Rahman RA, Hamid AA. 2007. Production of cyclodextrin glucanotransferase from alkalophilic Bacillus sp. TS1-1: Optimization of carbon and nitrogen concentration in the feed medium using central composite design. Biochem. Eng. J. 33: 26-33.
    CrossRef
  31. Leemhuis H, Kelly RM, Dijkhuizen L. 2010. Engineering of cyclodextrin glucanotransferases and the impact for biotechnological applications. Appl. Microbiol. Biotechnol. 85: 823-835.
    Pubmed KoreaMed CrossRef
  32. Park CS, Park KH, Kim SH. 1989. A rapid screening method for alkaline β-cyclodextrin glucanotransferase using phenolphthaleinmethyl orange-containingsolid medium. Agric. Biol. Chem. 53: 1167-1169.
    CrossRef
  33. Goel A, Nene SN. 1995. Modifications in the Phenolphthalein method for spectrophotometric estimation of beta cyclodextrin. Starch‐Stärke 47: 399-400.
    CrossRef
  34. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
    CrossRef
  35. Assis GBN, Pereira FL, Zegarra AU, Tavares GC, Leal CA, Figueiredo HCP. 2017. Use of MALDI-TOF mass spectrometry for the fast identification of gram-positive fish pathogens. Front. Microbiol. 8: 1492.
    Pubmed KoreaMed CrossRef
  36. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67: 1613-1617.
    Pubmed KoreaMed CrossRef
  37. Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874.
    Pubmed CrossRef
  38. Ferrarotti SA, Rosso AM, Maréchal MA, Krymkiewicz N, Maréchal LR. 1996. Isolation of two strains (S-R type) of Bacillus circulans and purification of a cyclomaltodextrin-glucanotransferase. Cell Mol. Biol. (Noisy-le-grand) 42: 653-657.
  39. Deng Z, Wang F, Zhou B, Li J, Li B, Liang H. 2019. Immobilization of pectinases into calcium alginate microspheres for fruit juice application. Food Hydrocoll. 89: 691-699.
    CrossRef
  40. Sophianopoulos AJ, Warner IM. 1992. Purification of beta-cyclodextrin. Anal. Chem. 64: 2652-2654.
    Pubmed CrossRef
  41. Tongnuanchan P, Benjakul S. 2014. Essential Oils: Extraction, bioactivities, and their uses for food preservation. J. Food Sci. 79: 1231-1249.
    Pubmed CrossRef
  42. Ayala-Zavala JF, Soto-Valdez H, González-León A, Álvarez-Parrilla E, Martín-Belloso O, González-Aguilar GA. 2008. Microencapsulation of cinnamon leaf (Cinnamomum zeylanicum) and garlic (Allium sativum) oils in β-cyclodextrin. J. Incl. Phenom. Macrocycl. Chem. 60: 359-368.
    CrossRef
  43. Ye Y, Zhu M, Miao K, Li X, Li D, Mu C. 2017. Development of antimicrobial gelatin-based edible films by incorporation of transanethole/β-cyclodextrin inclusion complex. Food Bioprocess Technol. 10: 1844-1853.
    CrossRef
  44. Lawrence HA, Palombo EA. 2009. Activity of essential oils against Bacillus subtilis spores. J. Microbiol. Biotechnol. 19: 1590-1595.
    Pubmed CrossRef
  45. Liang JB, Chen YQ, Lan CY, Tam NFY, Zan QJ, Huang LN. 2007. Recovery of novel bacterial diversity from mangrove sediment. Mar. Biol. 150: 739-747.
    CrossRef
  46. Mendes L, Tsai S, Mendes LW, Tsai SM. 2014. Variations of bacterial community structure and composition in mangrove sediment at different depths in southeastern Brazil. Diversity 6: 827-843.
    CrossRef
  47. Rahi P, Prakash O, Shouche YS. 2016. Matrix-assisted laser desorption/ionization time-of-flight Mass-Spectrometry (MALDI-TOF MS) based microbial identifications: challenges and scopes for microbial ecologists. Front. Microbiol. 7: 1359.
    Pubmed KoreaMed CrossRef
  48. Strejcek M, Smrhova T, Junkova P, Uhlik O. 2018. Whole-cell MALDI-TOF MS versus 16S rRNA gene analysis for identification and dereplication of recurrent bacterial isolates. Front. Microbiol. 9: 1294.
    Pubmed KoreaMed CrossRef
  49. Timperio AM, Gorrasi S, Zolla L, Fenice M. 2017. Evaluation of MALDI-TOF mass spectrometry and MALDI BioTyper in comparison to 16S rDNA sequencing for the identification of bacteria isolated from Arctic sea water. PLoS One 12: e0181860.
    Pubmed KoreaMed CrossRef
  50. Eş I, Ribeiro MC, dos Santos Júnior SR, Khaneghah AM, Rodriguez AG, Amaral AC. 2016. Production of cyclodextrin glycosyltransferase by immobilized Bacillus sp. on chitosan matrix. Bioprocess Biosyst. Eng. 39: 1487-1500.
    Pubmed CrossRef
  51. de Araújo Coelho SL, Magalhães VC, Marbach PAS, Cazetta ML. 2016. A new alkalophilic isolate of Bacillus as a producer of cyclodextrin glycosyltransferase using cassava flour. Braz. J. Microbiol. 47: 120-128.
    Pubmed KoreaMed CrossRef
  52. Blanco KC, De Lima CJB, Monti R, Martins J, Bernardi NS, Contiero J. 2012. Bacillus lehensis - An alkali-tolerant bacterium isolated from cassava starch wastewater: Optimization of parameters for cyclodextrin glycosyltransferase production. Ann. Microbiol. 62: 329-337.
    CrossRef
  53. Ivanova V. 2010. Immobilization of cyclodextrin glucanotransferase from Paenibacillus macerans atcc 8244 on magnetic carriers and production of cyclodextrins. Biotechnol. Biotechnol. Equip. 24: 516-528.
    CrossRef
  54. Reddy SV, More SS, Annappa GS. 2017. Purification and properties of beta-cyclomaltodextrin glucanotransferase from Bacillus flexus SV 1. J. Basic Microbiol. 57: 974-981.
    Pubmed CrossRef
  55. Mora MMM, Sánchez KH, Santana RV, Rojas AP, Ramírez HL, Torres-Labandeira JJ. 2012. Partial purification and properties of cyclodextrin glycosiltransferase (CGTase) from alkalophilic Bacillus species. Springerplus 1: 61.
    Pubmed KoreaMed CrossRef
  56. Li Y, Zhu C, Zhai X, Zhang Y, Duan Z, Sun J. 2018. Optimization of enzyme assisted extraction of polysaccharides from pomegranate peel by response surface methodology and their anti-oxidant potential. Chin. Herb Med. 10: 416-423.
    CrossRef
  57. Vijayaraghavan P, Arasu MV, Anantha Rajan R, Al-Dhabi NA. 2019. Enhanced production of fibrinolytic enzyme by a new Xanthomonas oryzae IND3 using low-cost culture medium by response surface methodology. Saudi J. Biol. Sci. 26: 217-224.
    Pubmed KoreaMed CrossRef
  58. Khan YM, Munir H, Anwar Z. 2019. Optimization of process variables for enhanced production of urease by indigenous Aspergillus niger strains through response surface methodology. Biocatal Agric. Biotechnol. 20: 101202.
    CrossRef
  59. Baş D, Boyacı İH. 2007. Modeling and optimization II: Comparison of estimation capabilities of response surface methodology with artificial neural networks in a biochemical reaction. J. Food Eng. 78: 846-854.
    CrossRef
  60. Vassileva A, Atanasova N, Ivanova V, Dhulster P, Tonkova A. 2007. Characterisation of cyclodextrin glucanotransferase from Bacillus circulans ATCC 21783 in terms of cyclodextrin production. Ann. Microbiol. 57: 609-615.
    CrossRef
  61. Costa H, Gastón JR, Lara J, Martinez CO, Moriwaki C, Matioli G, et al. 2015. Cyclodextrin glycosyltransferase production by free cells of Bacillus circulans DF 9R in batch fermentation and by immobilized cells in a semi-continuous process. Bioprocess Biosyst. Eng. 38: 1055-1063.
    Pubmed CrossRef
  62. Rajput KN, Patel KC, Trivedi UB. 2016. β-cyclodextrin production by cyclodextrin glucanotransferase from an alkaliphile Microbacterium terrae KNR 9 using different starch substrates. Biotechnol. Res. Int. 2016: 1-7.
    Pubmed KoreaMed CrossRef
  63. Schöffer JDN, Klein MP, Rodrigues RC, Hertz PF. 2013. Continuous production of β-cyclodextrin from starch by highly stable cyclodextrin glycosyltransferase immobilized on chitosan. Carbohydr. Polym. 98: 1311-1316.
    Pubmed CrossRef
  64. Ibrahim ASS, Al-Salamah AA, El-Toni AM, El-Tayeb MA, Elbadawi YB. 2014. Cyclodextrin glucanotransferase immobilization onto functionalized magnetic double mesoporous core-shell silica nanospheres. Electron. J. Biotechnol. 17: 55-64.
    CrossRef
  65. Matte CR, Nunes MR, Benvenutti EV, Schöffer J da N, Ayub MAZ, Hertz PF. 2012. Characterization of cyclodextrin glycosyltransferase immobilized on silica microspheres via aminopropyltrimethoxysilane as a “spacer arm.” J. Mol. Catal. B Enzym. 78: 51-56.
    CrossRef
  66. Kim MH, Sohn CB, Oh TK. 1998. Cloning and sequencing of a cyclodextrin glycosyltransferase gene from Brevibacillus brevis CD162 and its expression in Escherichia coli. FEMS Microbiol. Lett. 164: 411-418.
    Pubmed CrossRef
  67. Tonkova A. 1998. Bacterial cyclodextrin glucanotransferase. Enzyme Microb. Technol. 22: 678-686.
    CrossRef
  68. Kang J, Liu L, Wu X, Sun Y, Liu Z. 2018. Effect of thyme essential oil against Bacillus cereus planktonic growth and biofilm formation. Appl. Microbiol. Biotechnol. 102: 10209-10218.
    Pubmed CrossRef
  69. Shi C, Zhang X, Guo N. 2018. The antimicrobial activities and action-mechanism of tea tree oil against food-borne bacteria in fresh cucumber juice. Microb. Pathog. 125: 262-271.
    Pubmed CrossRef
  70. Quendera AP, Barreto AS, Semedo-Lemsaddek T. 2018. Antimicrobial activity of essential oils against foodborne multidrugresistant enterococci and aeromonads in planktonic and biofilm state. Food Sci. Technol. Int. 25: 101-108.
    Pubmed CrossRef
  71. Radünz M, da Trindade MLM, Camargo TM, Radünz AL, Borges CD, Gandra EA, et al. 2019. Antimicrobial and antioxidant activity of unencapsulated and encapsulated clove (Syzygium aromaticum, L.) essential oil. Food Chem. 276: 180-186.
    Pubmed CrossRef
  72. Celebioglu A, Yildiz ZI, Uyar T. 2018. Thymol/cyclodextrin inclusion complex nanofibrous webs: Enhanced water solubility, high thermal stability and antioxidant property of thymol. Food Res. Int. 106: 280-290.
    Pubmed CrossRef
  73. Abada MB, Hamdi SH, Gharib R, Messaoud C, Fourmentin S, Greige-Gerges H, et al. 2019. Post-harvest management control of Ectomyelois ceratoniae (Zeller) (Lepidoptera: Pyralidae): new insights through essential oil encapsulation in cyclodextrin. Pest Manag. Sci. 75: 2000-2008.
    Pubmed CrossRef
  74. Gadisa E, Weldearegay G, Desta K, Tsegaye G, Hailu S, Jote K, et al. 2019. Combined antibacterial effect of essential oils from three most commonly used Ethiopian traditional medicinal plants on multidrug resistant bacteria. BMC Complement Altern. Med. 19: 24.
    Pubmed KoreaMed CrossRef
  75. Pandini JA, Pinto FGS, Scur MC, Santana CB, Costa WF, Temponi LG, et al. 2017. Chemical composition, antimicrobial and antioxidant potential of the essential oil of Guarea kunthiana A. Juss. Braz. J. Biol. 78: 53-60.
    Pubmed CrossRef
  76. Herrera A, Rodríguez FJ, Bruna JE, Abarca RL, Galotto MJ, Guarda A, et al. 2019. Antifungal and physicochemical properties of inclusion complexes based on β-cyclodextrin and essential oil derivatives. Food Res. Int. 121: 127-135.
    Pubmed CrossRef
  77. Matshetshe KI, Parani S, Manki SM, Oluwafemi OS. 2018. Preparation, characterization and in vitro release study of β-cyclodextrin/chitosan nanoparticles loaded Cinnamomum zeylanicum essential oil. Int. J. Biol. Macromol. 118: 676-682.
    Pubmed CrossRef
  78. Chen G, Liu B. 2016. Cellulose sulfate based film with slowrelease antimicrobial properties prepared by incorporation of mustard essential oil and β-cyclodextrin. Food Hydrocoll. 55: 100- 107.
    CrossRef

Starts of Metrics

Share this article on :

  • mail

Related articles in MBL

Most KeyWord ?

What is Most Keyword?

  • It is most registrated keyword in articles at this journal during for 2 years.