Mechanism of action of an antifungal batercin produced by a marine Bacillus sp. Sh10
Subject Areas :
Microbial Biotechnology
fatemeh shayesteh
1
(Department of Fisheries, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran.)
Gires Usup
2
(School of Environmental Science and Natural Resources, Faculty of Science and Technology, University Kebangsaan Malaysia)
Received: 2021-12-10
Accepted : 2022-05-14
Published : 2022-06-05
Keywords:
Candida albicans,
Antifungal,
Bacillus sp,
bacteriocin,
marine bacteria,
Abstract :
Background and objective: bacteriocins are antimicrobial peptides produced by different bacteria and can be applied as a therapeutic agent. The aim of this study was to investigate the mode of action of broad-spectrum bacteriocin produced by a marine Bacillus, strain Sh10, on Candida albicans ATCC 10231.
Materials and Methods: Cell viability assay, determination of UV-absorbing materials, K+, inorganic phosphate, ATP, and LIVE/DEAD cell viability assay as well as scanned and transmission electron microscopy were used to investigate the mode of action of bacteriocin.
Results: The addition of 1 × MIC of bacteriocin to a cell suspension of C. albicans decreased the number of viable cells by about 4 log units over a period of 10 hours. It displayed a fungicidal mode of action with a massive leakage of K+ ions, inorganic phosphates, ATP, and UV-absorbance materials, leading to cell lysis. In addition, the permeability of C. albicans treated cells to propidium iodide was observed. The electron microscopic observations of treated cells indicated several modifications in cell morphology such as wrinkled surface, discontinuous and ruptured cell wall with concomitant lysis.
Conclusion: The data obtained in the current study demonstrated that the present bacteriocin interacted with the cytoplasmic membrane of C. albicans cells, resulting in pore formation, resulting in the efflux of interacellular materials that exhibit a fungicidal effect.
References:
References
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Mackenzie DWR, Cauwenberg G, Van Cutsem J, Drouhet E, Dupont B. Mycoses in AIDS patients: An overview.1990; New York, Plenum Press.
Friedman S, Richardson SE, Jacobs SE, O’Brien K. Systemic Candida infection in extremely low birth weight infants: Short term morbidity and neuro developmental outcome. The Pediatr Infect Dis J. 2000; 19 (6): 499-504.
Jarvis WR. Epidemiology of nosocomial fungal infections, with emphasis on Candida species. Clin Infect Dis. 1995; 20 (6): 1526-1530.
Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 2003; 11 (1): 30-36.
Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007; 20 (1): 133-63.
Arendrup MC, Sulim S, Holm A, Nielsen L, Nielsen SD, Knudsen JD, Drenck NE, Christensen JJ, Johansen HK. Diagnostic issues, clinical characteristics, and outcomes for patients with fungemia. J Clin Microbiol. 2011; 49 (9): 3300-3308.
Lai CC, Wang CY, Liu WL, Huang YT, Hsueh PR. Time to positivity of blood cultures of different Candida species causing fungaemia. J Med Microbiol. 2012; 61 (Pt 5):701-704.
Khan ZU, Chandy R, Metwali KE. Candida albicans strain carriage in patients and nursing staff of an intensive care unit: a study of morphotypes and resistotypes. Mycoses. 2003; 46 (11-12): 476-486.
Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 2002; 84 (5-6): 357-364.
Batoni G, Maisetta G, Brancatisano FL, Esin S, Campa M. Use of antimicrobial peptides against microbial biofilms: advantages and limits. Curr Med Chem. 2011; 18 (2): 256-279.
Okuda K, Zendo T, Sugimoto S, Iwase T, Tajima A, Yamada S, Sonomoto K, Mizunoe Y. Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother. 2013; 57 (11): 5572-5579.
Savadogo A, Ouattara CAT, Basole IHN, Traore SA. Bacteriocins and lactic acid bacteria: a mini-review. Afr J Biotechnol. 2006; 5 (9): 678-683.
O’ Sullivan LO, Ross PP, Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie. 2002; 84 (5-6): 593-604.
Shayesteh F, Ahmad A, Usup G. Bacteriocin production by a marine strain of Bacillus sp. Sh10: Isolation, screening and optimization of culture condition. Biotechnol. 2014; 13 (6): 273-281.
Shayesteh F, Ahmad A, Usup G. Partial Characterization of an Anti-Candida albicans Bacteriocin Produced by a Marine Strain of Bacillus sp., Sh10. Adv J Food Sci Technol. 2015; 9 (9): 664-671.
Pridham TG, Gottlieb D. The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol. 1948; 56 (1): 107-114.
Rajaram, G, Manivasagan P, Thilagavathi B, Saravanakumar A. Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. Adv J Food Sci Technol. 2010; 2 (2): 138-144.
Seuk-Hyun K, Cheol A. Bacteriocin production by Lactococcus lactis KCA 2386 isolated from white kimchi. Food Sci Biotechnol. 2000; 9: 263-269.
Clinical and Laboratory Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 6th edn. 2003; CLSI Document M7-A6: Wayne.
Motta AS, Flores FS, Souto AA, Brandelli A. Antibacterial activity of a bacteriocin-like substance produced by Bacillus sp. P34 that targets the bacterial cell envelope. Antonie Van Leeuwenhoek. 2008; 93 (3): 275-284.
Zhou K, Zhou W, Li P, Liu G, Zhang, J. Mode of action of pentocin 31-1: An antilisteria bacteriocin produced by Lactobacillus pentosus from Chinese traditional ham. Food Control. 2008; 19 (8): 817-22.
Ames BN. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1966; 8: 115-118.
Chen Y, Montville TJ. Efflux of ions and ATP depletion induced by pediocin PA-1 are concomitant with cell-death in Listeria monocytogenes Scott-A. J Appl Microbiol. 1995; 79 (6): 684-90.
Maurya IK, Pathak, S, Sharma M, Sanwa H, Chaudhary P, Tupe S, Deshpande M, Chauhan VS, Prasad R. Antifungal activity of novel synthetic peptides by accumulation of reactive oxygen species (ROS) and disruption of cell wall against Candida albicans. Peptides. 2011; 32 (8): 1732-1740.
Sharma A, Srivastava SH. Anti-Candida activity of two-peptide bacteriocins, plantaricins (Pln E/F and J/K) and their mode of action. Fungal Biol. 2014; 118 (2): 264-275.
Herranz C, Chen Y, Chung HJ, Cintas LM, Hernandez PE, Montville TJ, Chikindas ML. Enterocin P Selectively Dissipates the Membrane Potential of Enterococcus faecium T136. Appl Environ Microbiol. 2001; 67 (4): 1689-1692.
Fujita K, Ichimasa S, Zendo T, Koga S, Yoneyama F, Nakayama J, Sonomoto k. Structural Analysis and Characterization of Lacticin Q, a Novel Bacteriocin Belonging to a New Family of Unmodified Bacteriocins of Gram-Positive Bacteria. Appl Environ Microbiol. 2007; 73 (9): 2871-2877.
Gonzalez B, Glaasker E, Kunji ERS, Driessen AJM, Suarez JE. Bactericidal mode of action of plantaricin C. Appl Environ Microbiol. 1996; 62 (8): 2701-2709.
Yurong G, Dapeng L, Yan Sh, Xiaoyan L. Mode of action of sakacin C2 against Escherichia coli. Food Control. 2011; 22 (5): 657-661.
_||_References
Klepser ME. Antifungal resistance among Candida species. Pharmacotherapy. 2001; 21 (8 Pt 2): 124-132.
Mackenzie DWR, Cauwenberg G, Van Cutsem J, Drouhet E, Dupont B. Mycoses in AIDS patients: An overview.1990; New York, Plenum Press.
Friedman S, Richardson SE, Jacobs SE, O’Brien K. Systemic Candida infection in extremely low birth weight infants: Short term morbidity and neuro developmental outcome. The Pediatr Infect Dis J. 2000; 19 (6): 499-504.
Jarvis WR. Epidemiology of nosocomial fungal infections, with emphasis on Candida species. Clin Infect Dis. 1995; 20 (6): 1526-1530.
Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 2003; 11 (1): 30-36.
Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007; 20 (1): 133-63.
Arendrup MC, Sulim S, Holm A, Nielsen L, Nielsen SD, Knudsen JD, Drenck NE, Christensen JJ, Johansen HK. Diagnostic issues, clinical characteristics, and outcomes for patients with fungemia. J Clin Microbiol. 2011; 49 (9): 3300-3308.
Lai CC, Wang CY, Liu WL, Huang YT, Hsueh PR. Time to positivity of blood cultures of different Candida species causing fungaemia. J Med Microbiol. 2012; 61 (Pt 5):701-704.
Khan ZU, Chandy R, Metwali KE. Candida albicans strain carriage in patients and nursing staff of an intensive care unit: a study of morphotypes and resistotypes. Mycoses. 2003; 46 (11-12): 476-486.
Riley MA, Wertz JE. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 2002; 84 (5-6): 357-364.
Batoni G, Maisetta G, Brancatisano FL, Esin S, Campa M. Use of antimicrobial peptides against microbial biofilms: advantages and limits. Curr Med Chem. 2011; 18 (2): 256-279.
Okuda K, Zendo T, Sugimoto S, Iwase T, Tajima A, Yamada S, Sonomoto K, Mizunoe Y. Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother. 2013; 57 (11): 5572-5579.
Savadogo A, Ouattara CAT, Basole IHN, Traore SA. Bacteriocins and lactic acid bacteria: a mini-review. Afr J Biotechnol. 2006; 5 (9): 678-683.
O’ Sullivan LO, Ross PP, Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie. 2002; 84 (5-6): 593-604.
Shayesteh F, Ahmad A, Usup G. Bacteriocin production by a marine strain of Bacillus sp. Sh10: Isolation, screening and optimization of culture condition. Biotechnol. 2014; 13 (6): 273-281.
Shayesteh F, Ahmad A, Usup G. Partial Characterization of an Anti-Candida albicans Bacteriocin Produced by a Marine Strain of Bacillus sp., Sh10. Adv J Food Sci Technol. 2015; 9 (9): 664-671.
Pridham TG, Gottlieb D. The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol. 1948; 56 (1): 107-114.
Rajaram, G, Manivasagan P, Thilagavathi B, Saravanakumar A. Purification and characterization of a bacteriocin produced by Lactobacillus lactis isolated from marine environment. Adv J Food Sci Technol. 2010; 2 (2): 138-144.
Seuk-Hyun K, Cheol A. Bacteriocin production by Lactococcus lactis KCA 2386 isolated from white kimchi. Food Sci Biotechnol. 2000; 9: 263-269.
Clinical and Laboratory Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 6th edn. 2003; CLSI Document M7-A6: Wayne.
Motta AS, Flores FS, Souto AA, Brandelli A. Antibacterial activity of a bacteriocin-like substance produced by Bacillus sp. P34 that targets the bacterial cell envelope. Antonie Van Leeuwenhoek. 2008; 93 (3): 275-284.
Zhou K, Zhou W, Li P, Liu G, Zhang, J. Mode of action of pentocin 31-1: An antilisteria bacteriocin produced by Lactobacillus pentosus from Chinese traditional ham. Food Control. 2008; 19 (8): 817-22.
Ames BN. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1966; 8: 115-118.
Chen Y, Montville TJ. Efflux of ions and ATP depletion induced by pediocin PA-1 are concomitant with cell-death in Listeria monocytogenes Scott-A. J Appl Microbiol. 1995; 79 (6): 684-90.
Maurya IK, Pathak, S, Sharma M, Sanwa H, Chaudhary P, Tupe S, Deshpande M, Chauhan VS, Prasad R. Antifungal activity of novel synthetic peptides by accumulation of reactive oxygen species (ROS) and disruption of cell wall against Candida albicans. Peptides. 2011; 32 (8): 1732-1740.
Sharma A, Srivastava SH. Anti-Candida activity of two-peptide bacteriocins, plantaricins (Pln E/F and J/K) and their mode of action. Fungal Biol. 2014; 118 (2): 264-275.
Herranz C, Chen Y, Chung HJ, Cintas LM, Hernandez PE, Montville TJ, Chikindas ML. Enterocin P Selectively Dissipates the Membrane Potential of Enterococcus faecium T136. Appl Environ Microbiol. 2001; 67 (4): 1689-1692.
Fujita K, Ichimasa S, Zendo T, Koga S, Yoneyama F, Nakayama J, Sonomoto k. Structural Analysis and Characterization of Lacticin Q, a Novel Bacteriocin Belonging to a New Family of Unmodified Bacteriocins of Gram-Positive Bacteria. Appl Environ Microbiol. 2007; 73 (9): 2871-2877.
Gonzalez B, Glaasker E, Kunji ERS, Driessen AJM, Suarez JE. Bactericidal mode of action of plantaricin C. Appl Environ Microbiol. 1996; 62 (8): 2701-2709.
Yurong G, Dapeng L, Yan Sh, Xiaoyan L. Mode of action of sakacin C2 against Escherichia coli. Food Control. 2011; 22 (5): 657-661.
