Anti-Candida activity and industrial properties of Pediococcus pentosaceus NOA-2142 isolate from traditional pickled gherkin

Year 2022, , 494 - 501, 23.09.2022

Nilgün Özdemir

https://doi.org/10.31015/jaefs.2022.3.19

Abstract

Antifungal activities of LAB have increased in many environments, especially in foods, due to the harms of chemical preservatives, as they are natural and capable of preventing both spoilage and infections. This antifungal activity is associated with metabolic compounds of LAB such as cyclic dipeptides, fatty acids, hydrogen peroxide, organic acids, and phenyl lactic acid (PLA) which are produced directly or indirectly. On the other hand, many Candida sp. such as Candida albicans is an opportunistic pathogen and can cause diseases ranging from superficial mucosal to life-threatening systemic infections, and spoilage in food. Therefore, the anti-candida activity of LAB is an important issue. In this study, it was aimed to reveal the anti-candida activity of Pediococcus pentosaceus NOA-2142 which isolated from a traditional pickled gherkin, and to investigate the industrial properties of this strain for widespread use. In the study, the NOA-2142 isolate was selected for its high anti-candida activity, and was determined to belong to P. pentosaceus species. Subsequently, the minimum inhibitory concentration (MIC) of the cell-free supernatant (CFS) of this isolate against pathogen strains of Candida albicans and Candida tropicalis was determined as 1/128 and 1/64, respectively. In addition, the D-3-phenyllactic acid content, which is the most likely cause of the anti-candida activity of the CFS, was determined as 163.21 mg/L. Moreover, the isolate were revealed to have the ability to grow at temperatures of 15oC and above, and in the range of 3–12% NaCl concentration and 3.0–9 pH value. The NOA-2142 isolate showed the highest susceptibility with 40.53 mm zone diameter to the clindamycin antibiotic disc. As a result, the P. pentosaceus NOA-2142 with antifungal potential could be a proper candidate as bio-preservative starter or adjunct culture, or the CFS of P. pentosaceus NOA-2142 could be used as a natural additive.

Keywords

Anti-Candida activity, Pediococcus pentosaceus, D-3-phenyllactic acid, Growth conditions, Antibiotic activity

References

• Aarti, C., Khusro, A., Varghese, R., Arasu, M. V., Agastian, P., Al-Dhabi, N. A., Ilavenil, S., and Choi, K. C. (2018). In vitro investigation on probiotic, anti-Candida, and antibiofilm properties of Lactobacillus pentosus strain LAP1. Archives of Oral Biology, 89(January), 99–106. https://doi.org/10.1016/j.archoralbio.2018.02.014
• Akoğlu, A., Yaman, H., Coşkun, H., and Sarı, K. (2016). Mengen Peynirinden Laktik Asit Bakterilerinin İzolasyonu, Moleküler Tanımlanması ve Bazı Starter Kültür Özelliklerinin Belirlenmesi. Süleyman Demirel Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 21(2), 453. (in Turkish) https://doi.org/10.19113/sdufbed.11073
• Bamidele, T. A., Adeniyi, B. A., and Smith, S. I. (2019). In vitro, acidic, non-proteinaceous antifungal activities of lactic acid bacteria isolated from salad vegetables against human pathogenic Candida albicans. African Journal of Clinical and Experimental Microbiology, 20(2), 137. https://doi.org/10.4314/ajcem.v20i2.7
• Bulgasem, B. Y., Lani, M. N., Hassan, Z., Wan Yusoff, W. M., and Fnaish, S. G. (2016). Antifungal activity of lactic acid bacteria strains isolated from natural honey against Pathogenic Candida species. Mycobiology, 44(4), 302–309. https://doi.org/10.5941/MYCO.2016.44.4.302
• Bustos, A. Y., Font de Valdez, G., and Gerez, C. L. (2018). Optimization of phenyllactic acid production by Pediococcus acidilactici CRL 1753. Application of the formulated bio-preserver culture in bread. Biological Control, 123(January), 137–143. https://doi.org/10.1016/j.biocontrol.2018.05.017
• Cizeikiene, D., Juodeikiene, G., Paskevicius, A., and Bartkiene, E. (2013). Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control, 31(2), 539–545. https://doi.org/10.1016/j.foodcont.2012.12.004
• CLSI; Clinical and Laboratory Standards Institute. (2002). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi. M38. Clinical and Laboratory Standards Institute, Wayne, PA. Retrieved from: https://clsi.org/media/1894/m38ed3_sample.pdf
• CLSI; Clinical and Laboratory Standards Institute. (2008). Reference method Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts and corresponding supplement M60-M27-M44. Clinical and Laboratory Standards Institute, Wayne, PA. Retrieved from: https://clsi.org/media/1895/m60ed1_sample.pdf
• Coloretti, F., Carri, S., Armaforte, E., Chiavari, C., Grazia, L., and Zambonelli, C. (2007). Antifungal activity of lactobacilli isolated from salami. FEMS Microbiology Letters, 271(2), 245–250. https://doi.org/10.1111/j.1574-6968.2007.00723.x
• Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., and García, H. S. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. International Journal of Food Microbiology, 173, 30–35. https://doi.org/10.1016/j.ijfoodmicro.2013.12.016
• Crowley, S., Mahony, J., and Van Sinderen, D. (2013). Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends in Food Science and Technology, 33(2), 93–109. https://doi.org/10.1016/j.tifs.2013.07.004
• Danielsen, M., Simpson, P. J., O’Connor, E. B., Ross, R. P., and Stanton, C. (2007). Susceptibility of Pediococcus spp. to antimicrobial agents. Journal of Applied Microbiology, 102(2), 384–389. https://doi.org/10.1111/j.1365-2672.2006.03097.x
• Diguță, C. F., Nițoi, G. D., Matei, F., Luță, G., and Cornea, C. P. (2020). The biotechnological potential of pediococcus spp. Isolated from kombucha microbial consortium. Foods, 9(12). https://doi.org/10.3390/foods9121780
• G-Alegría, E., López, I., Ruiz, J. I., Sáenz, J., Fernández, E., Zarazaga, M., Dizy, M., Torres, C., and Ruiz-Larrea, F. (2004). High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiology Letters, 230(1), 53–61. https://doi.org/10.1016/S0378-1097(03)00854-1
• Huang, J., Li, S., Wang, Q., Guan, X., Qian, L., Li, J., Zheng, Y., and Lin, B. (2020). Pediococcus pentosaceus B49 from human colostrum ameliorates constipation in mice. Food and Function, 11(6), 5607–5620. https://doi.org/10.1039/d0fo00208a
• Ilavenil, S., Vijayakumar, M., Kim, D. H., Valan Arasu, M., Park, H. S., Ravikumar, S., and Choi, K. C. (2016). Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian ryegrass. Journal of the Science of Food and Agriculture, 96(2), 593–601. https://doi.org/10.1002/jsfa.7128
• Kaya, H. İ., and Şimşek, Ö. (2020). Characterization of Pediococcus acidilactici PFC69 and Lactococcus lactis PFC77 bacteriocins and their antimicrobial activities in tarhana fermentation. Microorganisms, 8(7), 1–13. https://doi.org/10.3390/microorganisms8071083
• Köhler, G. A., Assefa, S., and Senait, G. (2012). Probiotic Interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the Opportunistic Fungal Pathogen Candida albicans. Hindawi Publishing Corporation Infectious Diseases in Obstetrics and Gynecology, 41(4), 687–690. https://doi.org/10.1155/2012/636474
• Kuppusamy, P., Kim, D., Soundharrajan, I., Park, H. S., Jung, J. S., Yang, S. H., and Choi, K. C. (2020). Low-carbohydrate tolerant LAB strains identified from rumen fluid: Investigation of probiotic activity and legume silage fermentation. Microorganisms, 8(7), 1–17. https://doi.org/10.3390/microorganisms8071044
• Li, X., Jiang, B., and Pan, B. (2007). Biotransformation of phenylpyruvic acid to phenyllactic acid by growing and resting cells of a Lactobacillus sp. Biotechnology Letters, 29(4), 593–597. https://doi.org/10.1007/s10529-006-9275-4
• Lu, X., Rasco, B. A., Kang, D. H., Jabal, J. M. F., Aston, D. E., and Konkel, M. E. (2011). Infrared and Raman spectroscopic studies of the antimicrobial effects of garlic concentrates and diallyl constituents on foodborne pathogens. Analytical Chemistry, 83(11), 4137–4146. https://doi.org/10.1021/ac2001498
• Mu, W., Yu, S., Zhu, L., Jiang, B., and Zhang, T. (2012a). Production of 3-phenyllactic acid and 4-hydroxyphenyllactic acid by Pediococcus acidilactici DSM 20284 fermentation. European Food Research and Technology, 235(3), 581–585. https://doi.org/10.1007/s00217-012-1768-x
• Mu, W., Yu, S., Zhu, L., Zhang, T., and Jiang, B. (2012b). Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound. Applied Microbiology and Biotechnology, 95(5), 1155–1163. https://doi.org/10.1007/s00253-012-4269-8
• Nasrollahzadeh, A., Mokhtari, S., Khomeiri, M., and Saris, P. E. J. (2022). Antifungal Preservation of Food by Lactic Acid Bacteria. Foods, 11(3), 1–18. https://doi.org/10.3390/foods11030395
• Papon, N., Courdavault, V., Clastre, M., and Bennett, R. J. (2013). Emerging and Emerged Pathogenic Candida Species: Beyond the Candida albicans Paradigm. PLoS Pathogens, 9(9). https://doi.org/10.1371/journal.ppat.1003550
• Pemán, J., Cantón, E., and Espinel-Ingroff, A. (2009). Antifungal drug resistance mechanisms. Expert Review of Anti-Infective Therapy, 7(4), 453–460. https://doi.org/10.1586/ERI.09.18
• Plessas, S., Nouska, C., Karapetsas, A., Kazakos, S., Alexopoulos, A., Mantzourani, I., Chondrou, P., Fournomiti, M., Galanis, A., and Bezirtzoglou, E. (2017). Isolation, characterization and evaluation of the probiotic potential of a novel Lactobacillus strain isolated from Feta-type cheese. Food Chemistry, 226, 102–108. https://doi.org/10.1016/J.FOODCHEM.2017.01.052
• Qi, Y., Huang, L., Zeng, Y., Li, W., Zhou, D., Xie, J., Xie, J., Tu, Q., Deng, D., and Yin, J. (2021). Pediococcus pentosaceus: Screening and Application as Probiotics in Food Processing. Frontiers in Microbiology, 12(December). https://doi.org/10.3389/fmicb.2021.762467
• Ramage, G., Saville, S. P., Thomas, D. P., and López-Ribot, J. L. (2005). Candida biofilms: An update. Eukaryotic Cell, 4(4), 633–638. https://doi.org/10.1128/EC.4.4.633-638.2005
• Salari, S., and Ghasemi Nejad Almani, P. (2020). Antifungal effects of Lactobacillus acidophilus and Lactobacillus plantarum against different oral Candida species isolated from HIV/ AIDS patients: an in vitro study. Journal of Oral Microbiology, 12(1). https://doi.org/10.1080/20002297.2020.1769386
• Schnürer, J., and Magnusson, J. (2005). Antifungal lactic acid bacteria as biopreservatives. Trends in Food Science and Technology, 16(1–3), 70–78. https://doi.org/10.1016/j.tifs.2004.02.014
• Schwenninger, S. M., Lacroix, C., Truttmann, S., Jans, C., Spörndli, C., Bigler, L., and Meile, L. (2008). Characterization of low-molecular-weight antiyeast metabolites produced by a food-protective Lactobacillus-Propionibacterium coculture. Journal of Food Protection, 71(12), 2481–2487. https://doi.org/10.4315/0362-028X-71.12.2481
• Schwenninger, S. M., and Meile, L. (2004). A Mixed Culture of Propionibacterium jensenii and Lactobacillus paracasei subsp. paracasei Inhibits Food Spoilage Yeasts. Systematic and Applied Microbiology, 27(2), 229–237. https://doi.org/10.1078/072320204322881853
• Sellamani, M., Kalagatur, N. K., Siddaiah, C., Mudili, V., Krishna, K., Natarajan, G., and Rao Putcha, V. L. (2016). Antifungal and zearalenone inhibitory activity of Pediococcus pentosaceus isolated from dairy products on Fusarium graminearum. Frontiers in Microbiology, 7(JUN), 1–12. https://doi.org/10.3389/fmicb.2016.00890 Shani, N., Oberhaensli, S., and Arias-Roth, E. (2021). Antibiotic susceptibility profiles of Pediococcus pentosaceus from various origins and their implications for the safety assessment of strains with food-technology applications. Journal of Food Protection, 84(7), 1160–1168. https://doi.org/10.4315/JFP-20-363
• Yoo, J. A., Lim, Y. M., and Yoon, M. H. (2016). Production and antifungal effect of 3-phenyllactic acid (PLA) by lactic acid bacteria. Journal of Applied Biological Chemistry, 59(3), 173–178. https://doi.org/10.3839/jabc.2016.032
• Yu, S., Jiang, H., Jiang, B., and Mu, W. (2012). Characterization of D-lactate dehydrogenase producing D-3-phenyllactic acid from Pediococcus pentosaceus. Bioscience, Biotechnology and Biochemistry, 76(4), 853–855. https://doi.org/10.1271/bbb.110955
• Yu, S., Zhou, C., Zhang, T., Jiang, B., and Mu, W. (2015). 3-Phenyllactic acid production in milk by Pediococcus pentosaceus SK25 during laboratory fermentation process. Journal of Dairy Science, 98(2), 813–817. https://doi.org/10.3168/jds.2014-8645