DOI QR코드

DOI QR Code

Antifungal Activity of Lactic Acid Bacteria Strains Isolated from Natural Honey against Pathogenic Candida Species

  • Bulgasem, Bulgasem Y. (Department of Microbiology, Faculty of Science and Technology, Universiti Sains Islam Malaysia (USIM)) ;
  • Lani, Mohd Nizam (School of Food Science and Technology, Universiti Malaysia Terengganu (UMT)) ;
  • Hassan, Zaiton (Department of Microbiology, Faculty of Science and Technology, Universiti Sains Islam Malaysia (USIM)) ;
  • Yusoff, Wan Mohtar Wan (School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia) ;
  • Fnaish, Sumaya G. (Department of Community Health, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia)
  • Received : 2016.02.23
  • Accepted : 2016.11.30
  • Published : 2016.12.30

Abstract

The role of lactic acid bacteria (LAB) in honey as antifungal activity has received little attention and their mechanism of inhibitory of fungi is not fully understood. In this study, LAB were isolated from honey samples from Malaysia, Libya, Saudi Arabia, and Yemen. Twenty-five isolates were confirmed LAB by catalase test and Gram staining, and were screened for antifungal activity. Four LAB showed inhibitory activity against Candida spp. using the dual agar overlay method. And they were identified as Lactobacillus plantarum HS isolated from Al-Seder honey, Lactobacillus curvatus HH isolated from Al-Hanon honey, Pediococcus acidilactici HC isolated from Tualang honey and Pediococcus pentosaceus HM isolated from Al-Maray honey by the 16S rDNA sequence. The growth of Candida glabrata ATCC 2001 was strongly inhibited (>15.0 mm) and (10~15 mm) by the isolates of L. curvatus HH and P. pentosaceus HM, respectively. The antifungal activity of the crude supernatant (cell free supernatant, CFS) was evaluated using well diffusion method. The CFS showed high antifungal activity against Candida spp. especially The CFS of L. curvatus HH was significantly (p < 0.05) inhibited growth of C. glabrata ATCC 2001, C. parapsilosis ATCC 2201, and C. tropicalis ATCC 750 with inhibitory zone 22.0, 15.6, and 14.7 mm, respectively. While CFS of P. pentosaceus HM was significantly (p < 0.05) effective against C. krusei, C. glabrata, and C. albicans with inhibition zone 17.2, 16.0, and 13.3 mm, respectively. The results indicated that LAB isolated from honey produced compounds which can be used to inhibit the growth of the pathogenic Candida species.

Keywords

References

  1. Weston RJ, Brocklebank LK. The oligosaccharide composition of some New Zealand honeys. Food Chem 1999;64:33-7. https://doi.org/10.1016/S0308-8146(98)00099-5
  2. Molan P. The antibacterial properties of honey. Chem N Z 1995;59:10-4.
  3. Endo A, Futagawa-Endo Y, Dicks LM. Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst Appl Microbiol 2009;32:593-600. https://doi.org/10.1016/j.syapm.2009.08.002
  4. Adeniyi BA, Ayeni FA, Ogunbanwo ST. Antagonistic activities of lactic acid bacteria isolated from Nigerian fermented dairy food against organisms implicated in urinary tract infection. Biotechnology 2006;5:183-8. https://doi.org/10.3923/biotech.2006.183.188
  5. Sezer C, Guven A. Investigation of bacteriocin production capability of lactic acid bacteria isolated from foods. Kafkas Univ Vet Fak Derg 2009;15:45-50.
  6. Suskovic J, Kos B, Beganovic J, Lebos Pavunc A, Habjanic K, Matosic S. Antimicrobial activity: the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotechnol 2010;48:296-307.
  7. Carlson P, Richardson M, Paavonen J. Evaluation of the Oricult-N dipslide for laboratory diagnosis of vaginal candidiasis. J Clin Microbiol 2000;38:1063-5.
  8. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 2001;183:5385-94. https://doi.org/10.1128/JB.183.18.5385-5394.2001
  9. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol 2003;11:30-6. https://doi.org/10.1016/S0966-842X(02)00002-1
  10. Ramage G, Martinez JP, Lopez-Ribot JL. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 2006;6:979-86. https://doi.org/10.1111/j.1567-1364.2006.00117.x
  11. Mishra NN, Prasad T, Sharma N, Payasi A, Prasad R, Gupta DK, Singh R. Pathogenicity and drug resistance in Candida albicans and other yeast species: a review. Acta Microbiol Immunol Hung 2007;54:201-35. https://doi.org/10.1556/AMicr.54.2007.3.1
  12. Sanguinetti M, Posteraro B, Lass-Florl C. Antifungal drug resistance among Candida species: mechanisms and clinical impact. Mycoses 2015;58 Suppl 2:2-13.
  13. Pikman R, Ben-Ami R. Immune modulators as adjuncts for the prevention and treatment of invasive fungal infections. Immunotherapy 2012;4:1869-82. https://doi.org/10.2217/imt.12.127
  14. Girmenia C, Menichetti F. Antimicrobial prophylaxis in hematology. In: Maschmeyer G, Rolston KV, editors. Infections in hematology. Berlin: Springer; 2015. p. 275-96.
  15. Kaskoniene V, Venskutonis PR. Floral markers in honey of various botanical and geographic origins: a review. Compr Rev Food Sci Food Saf 2010;9:620-34. https://doi.org/10.1111/j.1541-4337.2010.00130.x
  16. Moussa A, Saad A, Djebli ND, Meslem A, Benhalima AE. Antifungal activity of four honeys of different types from Algeria against pathogenic yeast: Candida albicans and Rhodotorula sp. Int J Microbiol Res 2011;2:276-9.
  17. Omafuvbe BO, Akanbi OO. Microbiological and physico-chemical properties of some commercial Nigerian honey. Afr J Microbiol Res 2009;3:891-6.
  18. Koc AN, Silici S, Ercal BD, Kasap F, Hormet-Oz HT, Mavus-Buldu H. Antifungal activity of Turkish honey against Candida spp. and Trichosporon spp: an in vitro evaluation. Med Mycol 2009;47:707-12. https://doi.org/10.3109/13693780802572554
  19. Bulgasem BY, Hassan Z, Abdalsadiq NK, Yousoff WM, Musa EM, Lani MN. Anti-adhesion activity of lactic acid bacteria supernatant against human pathogenic Candida species biofilm. Health Sci J 2015;9:3.
  20. De Man JC, Rogosa M, Sharpe ME. A medium for the cultivation of Lactobacilli. J Appl Bacteriol 1960;23:130-5. https://doi.org/10.1111/j.1365-2672.1960.tb00188.x
  21. Panthavee W, Saithong P, Worawuthiyana N. Identification and evaluation of lactic acid bacteria for Pla-som (fermented fish) starter. In: The 2nd International Conference on Fermentation Technology for Value Added Agricultural Products; 2007 May 23-25; Khon Kaen, Thailand.
  22. Ogunbanwo ST. Functional properties of lactic acid bacteria isolated from Ogi and Fufu, two Nigerian fermented foods. Adv Food Sci 2005;27:14-21.
  23. Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966;45:493-6. https://doi.org/10.1093/ajcp/45.4_ts.493
  24. Subramani S, Vignesh S. MAR index study and MDR character analysis of a few golden staph isolates. Asian J Pharm Life Sci 2012;2:151-4.
  25. Magnusson J, Schnurer J. Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Appl Environ Microbiol 2001;67:1-5. https://doi.org/10.1128/AEM.67.1.1-5.2001
  26. Tamminen M, Joutsjoki T, Sjoblom M, Joutsen M, Palva A, Ryhanen EL, Joutsjoki V. Screening of lactic acid bacteria from fermented vegetables by carbohydrate profiling and PCR-ELISA. Lett Appl Microbiol 2004;39:439-44. https://doi.org/10.1111/j.1472-765X.2004.01607.x
  27. Magnusson J, Strom K, Roos S, Sjogren J, Schnurer J. Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol Lett 2003;219:129-35. https://doi.org/10.1016/S0378-1097(02)01207-7
  28. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792-7. https://doi.org/10.1093/nar/gkh340
  29. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406-25.
  30. Ruiz-Argueso T, Rodriguez-Navarro A. Microbiology of ripening honey. Appl Microbiol 1975;30:893-6.
  31. Bahiru B, Mehari T, Ashenafi M. Yeast and lactic acid flora of tej, an indigenous Ethiopian honey wine: variations within and between production units. Food Microbiol 2006;23:277-82. https://doi.org/10.1016/j.fm.2005.05.007
  32. Hosny I, El-Ghani SA, Nadir AS. Nutrient composition and microbiological quality of three unifloral honeys with emphasis on processing of honey probiotic youghurt. Glob Vet 2009;3:107-12.
  33. Forsgren E, Olofsson TC, Vaasquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 2010;41:99-108. https://doi.org/10.1051/apido/2009065
  34. Aween MM, Hassan Z, Muhialdin BJ, Eljamel YA, Al-Mabrok AS, Lani MN. Antibacterial activity of Lactobacillus acidophilus strains isolated from honey marketed in Malaysia against selected multiple antibiotic resistant (MAR) gram-positive bacteria. J Food Sci 2012;77:M364-71. https://doi.org/10.1111/j.1750-3841.2012.02776.x
  35. Atanassova M, Choiset Y, Dalgalarrondo M, Chobert JM, Dousset X, Ivanova I, Haertle T. Isolation and partial biochemical characterization of a proteinaceous anti-bacteria and anti-yeast compound produced by Lactobacillus paracasei subsp. paracasei strain M3. Int J Food Microbiol 2003;87:63-73. https://doi.org/10.1016/S0168-1605(03)00054-0
  36. Jin L, Tao L, Pavlova SI, So JS, Kiwanuka N, Namukwaya Z, Saberbein BA, Wawer M. Species diversity and relative abundance of vaginal lactic acid bacteria from women in Uganda and Korea. J Appl Microbiol 2007;102:1107-15.
  37. Ogunshe AA, Omotoso MA, Bello VB. The in vitro antimicrobial activities of metabolites from Lactobacillus strains on Candida species implicated in Candida vaginitis. Malays J Med Sci 2011;18:13-25.
  38. Cizeikiene D, Juodeikiene G, Paskevicius A, Bartkiene E. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control 2013;31:539-45. https://doi.org/10.1016/j.foodcont.2012.12.004
  39. Adeniyi B, Iveren D. Antifungal capacity of lactic acid bacteria isolated from salad vegetables. Afr J Biomed Res 2011;14:137-41.
  40. Oluwafemi F, Adetunji AF. Antimicrobial activities of lactic acid bacteria isolated from traditionally-fermented maize (ogi) against Candida albicans. J Appl Biosci 2011;41:2820-35.
  41. Laref N, Guessas B. Antifungal activity of newly isolates of lactic acid bacteria. Innov Rom Food Biotechnol 2013;13:80-8.
  42. Muhialdin BJ, Hassan Z, Sadon SK. Antifungal activity of Lactobacillus fermentum Te007, Pediococcus pentosaceus Te010, Lactobacillus pentosus G004, and L. paracasi D5 on selected foods. J Food Sci 2011;76:M493-9. https://doi.org/10.1111/j.1750-3841.2011.02292.x
  43. Al-Abeid HM, Abu-Elteen KH, Elkarmi AZ, Hamad MA. Isolation and characterization of Candida spp. in Jordanian cancer patients: prevalence, pathogenic determinants, and antifungal sensitivity. Jpn J Infect Dis 2004;57:279-84.
  44. Lertcanawanichakul M. Isolation and selection of anti-Candida albicans producing lactic acid bacteria. Walailak J Sci Technol 2005;2:179-87.
  45. Verdenelli MC, Ghelfi F, Silvi S, Orpianesi C, Cecchini C, Cresci A. Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. Eur J Nutr 2009;48:355-63. https://doi.org/10.1007/s00394-009-0021-2
  46. Kariptas E, Tulumoglu S, Erdem B. Antifungal effects of Lactobacillus spp. bacteria on Candida yeast. Kafkas Univ Vet Fak Derg 2010;16:1061-4.
  47. Chew SY, Cheah YK, Seow HF, Sandai D, Than LT. Probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 exhibit strong antifungal effects against vulvovaginal candidiasis-causing Candida glabrata isolates. J Appl Microbiol 2015;118:1180-90. https://doi.org/10.1111/jam.12772
  48. Ronnqvist D, Forsgren-Brusk U, Husmark U, Grahn-Hakansson E. Lactobacillus fermentum Ess-1 with unique growth inhibition of vulvo-vaginal candidiasis pathogens. J Med Microbiol 2007;56(Pt 11):1500-4. https://doi.org/10.1099/jmm.0.47226-0
  49. Sungsri T, Lertcanawanichakul M, Siwayaprahm P. Isolation and selection of anti-Candida albicans metabolites producing lactic acid bacteria from various sources. KKU Res J 2012;17:630-8.
  50. Olofsson TC, Alsterfjord M, Nilson B, Butler E, Vasquez A. Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol 2014;64(Pt 9):3109-19. https://doi.org/10.1099/ijs.0.059600-0