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Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates

Yıl 2023, Cilt: 27 Sayı: 6, 2374 - 2388, 28.06.2025

Nurten Tetik Pervin Rayaman , Erkan Rayaman , Rıza Adaleti

Öz

In this study we aimed to identify probiotic microorganisms in various pharmacy preparations, market and homemade probiotic products and investigate the antimicrobial effect of these microorganisms on clinical and standard Staphylococcus aureus isolates. The probiotic microorganisms were isolated from probiotic products mentioned above, then identified by Matrix Assisted Laser Ionization Mass Spectrophotometer (MALDI-TOF, Biomeriux) and also by conventional methods. The tolerance of these probiotic microorganisms to different salt, pH and temperature conditions was also detected. The antimicrobial activity of the specified probiotic microorganisms on S. aureus was designated by using spot on lawn and agar well diffusion methods. In our study among 16 probiotic products, 27 various probiotic microorganisms were specified by MALDI-TOF. Additionally, 15 of these probiotic microorganism species had an isolated reliability value above 90%. In our study 10 probiotic microorganism species, 7 of which were different from each other were found to maintain their viability in three various pH, salt and temperature conditions. These probiotic microorganisms were Lactobacillus rhamnosus (P.2 probiotic pharmaceutical product), Enterococcus gallinarum (homemade whey), Lactobacillus kefiri 1 (homemade kefir), Bacillus megaterium (homemade pickled juice), Lactobacillus kefiri 2 (homemade kefir), Lactobacillus rhamnosus (P.1 company preparation) Lactobacillus plantarum (P.3 company preparation), Bifidobacterium spp (M.4 company pure kefir), Enterococcus faecium (P.3 company preparation). We determined that Lactobacillus plantarum isolated from homemade whey had the highest antimicrobial activity on clinical MRSA 3 (Methicillin resistant Staphylococcus aureus) strain (inhibition zone =45.62 mm ± 0.84. Also, we have found that, probiotic microorganisms isolated from pharmacy preparations, market and homemade probiotic products showed antibacterial effect on clinical and standard Staphylococcus aureus by spot on lawn method. We designated that besides probiotic microorganisms isolated from various pharmacy preparations, probiotic microorganisms isolated from market and homemade products were efficient against clinical and standard S. aureus isolates.

Anahtar Kelimeler

Probiotic products antimicrobial activity probiotic microorganisms Staphylococcus aureus spot on lawn

Kaynakça

  • [1] Compare D, Sgamato C, Nardone OM, Rocco A, Coccoli P, Laurenza C, Nardone G. Probiotics in gastrointestinal diseases: All that glitters is not gold. Dig Dis. 2022;40(1):123-132. https://doi.org/10.1159/000516023.
  • [2] Ghannoum MA, McCormick TS, Retuerto M, Bebek G, Cousineau S, Hartman L, Barth C, Schrom K. Evaluation of microbiome alterations following consumption of BIOHM, a novel probiotic. Curr Issues Mol Biol. 2021;43(3):2135-2146. https://doi.org/10.3390/cimb43030148
  • [3] Hashim ZA. Evaluation of bacterial contents, package labelling and antimicrobial activity of some commercial probiotic products available in local market. J Res Pharm. 2022;26(3):502-509. http://dx.doi.org/10.29228/jrp.147
  • [4] Castellone V, Bancalari E, Rubert J, Gatti M, Neviani E, Bottari B. Eating fermented: Health benefits of LAB-fermented foods. Foods. 2021;10(11):26-39. https://doi.org/10.3390/foods10112639
  • [5] Ouwehand AC, Vesterlund S. Antimicrobial components from lactic acid bacteria. In: Salminen S, (ed). Lactic Acid Bacteria. 3rd edn. Marcel Dekker, New York, 2004, pp 375-397.
  • [6] Ong JS, Taylor TD, Yong CC, Khoo BY, Sasidharan S, Choi SB, Ohno H, Liong MT. Lactobacillus plantarum USM8613 aids in wound healing and suppresses Staphylococcus aureus infection at wound sites. Probiotics Antimicrob Proteins. 2020;12(1):125-137. https://doi.org/10.1007/s12602-018-9505-9
  • [7] Dinçer, E., Kıvanç, M. Invitro evaluation of probiotic potential of Enterococcus faecium strains isolated from Turkish pastırma. Archives of Microbiology. 2021;203(6), 2831-2841. https://doi.org/10.1007/s00203-021-02273-y.
  • [8] Yoha KS, Nida S, Dutta S, Moses JA, Anandharamakrishnan C. Targeted delivery of probiotics: perspectives on research and commercialization. Probiotics Antimicrob Proteins. 2021;27:1-34. https://doi.org/10.1007/s12602-021-09791-7
  • [9] Yılmaz M, Şeker E. Investigation of mecA, vanA and PVL genes in Staphylococcus aureus strains isolated from bovine mastitis in small holder dairy farms. Etlik Vet Mikrobiyol Derg. 2022;33(1):50-55. https://doi.org/10.35864/evmd.1008728
  • [10] Alışkan HE, Başustaoğlu A. Determination of biofilm formation properties of methicillin sensitive and resistant Staphylococcus aureus isolates by conventional and molecular methods. Mikrobiyoloji Bul. 2020;54(2):223-234. https://doi.org/10.5578/mb.69204
  • [11] Park S, Classen A, Gohou HM, Maldonado R, Kretschmann E, Duvernay C, Kim GK, Ronholm J. A new, reliable, and high-throughput strategy to screen bacteria for antagonistic activity against Staphylococcus aureus. BMC Microbiol. 2021;21(1):189. https://doi.org/10.1186/s12866-021-02265-4
  • [12] Mazzantini D, Celandroni F, Calvigioni M, Panattoni A, Labella R, Ghelardi E. Microbiological Quality and Resistance to an Artificial Gut Environment of Two Probiotic Formulations. Foods. 2021;10(11):2781. https://doi.org/10.3390/foods10112781
  • [13] Rolfe RD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr. 2000;130:396-402. https://doi.org/10.1093/jn/130.2.396S
  • [14] Çoşkun T. Probiotics. In: Kara A, Çoşkun T (eds) Prebiotics and probiotics from theory to clinic. Ömür Typography AC, İstanbul, 2014, pp:56-7.
  • [15] Durak Y, Uysal A, Aladağ MO, Akın D. Ticari yoğurt örneklerinden canlı laktik asit bakterilerinin izolasyonu ve sayımı (Isolation and counting of live lactic acid bacteria from commercial yogurt samples). SUFEFD. 2015;41:83-88.
  • [16] Dumani A, Yoldaş O, Akçimen B, Yılmaz Ş, Köksal F. Farklı çeşitteki Türk peynirlerinde Enterococcus faecalis türünün tespiti. Atatürk Üniv Diş Hek Fak Derg. 2015;25(1):35-9. https://doi.org/10.17567/dfd.97125
  • [17] Tomar O, Çağlar A, Akarca G. Kefir ve sağlık açısından önemi. AKÜ FEMÜBİD. 2017;17(2):834-853. https://doi.org/10.5578/fmbd.57533
  • [18] Çelikel A, Göncü B, Akın MB, Akın MS. Süt ürünlerinde probiyotik bakterilerin canlılığını etkileyen faktörler. Batman Üniversitesi Yaşam Bilimleri Dergisi. 2018;8(1/2):59-68.
  • [19] Schillinger U, Lucke FK. Antibacterial activity of Lactobacillus sakei isolated from meat. Appl Environ Microbiol. 1989;5(8):1901-1906. https://doi.org/10.1128/aem.55.8.1901-1906.1989
  • [20] Özdemir H, Küplülü Ö, Çelik HT. Determination of antibacterial effects of Lactobacilli isolated from Turkish Fermented Sausage. Gıda. 2002;27(6):539-544.
  • [21] Tuncer Y, Özden B, Akçelik M. Lactococcus lactis subsp. from tulum cheese partial characterization of bacteriocins produced by lactis YBML9 and YBML21 strains. SDÜ Fen Bil Enst Der. 2008;12(2):141-148.
  • [22] Goderska K, Czarnecki Z. Characterization of selected strains from Lactobacillus acidophilus and Bifidobacterium bifidum. Afr J Microbiol Res. 2007;1(6):65-78.
  • [23] Altuntaş EG, Ayhan K, Okcu G, Erkanlı K, Balcı MH, Sonakın ŞS. Antimicrobial activities of lactic acid bacteria isolated from raw milk and cheese samples. Gıda. 2010;35(3):197-203.
  • [24] Hassan M, Javadzadeh Y, Lotfipour F, Badomchi R. Determination of comparative minimum inhibitory concentration (MIC) of bacteriocins produced by enterococci for selected isolates of multi-antibiotic resistant Enterococcus spp. Adv Pharm Bull. 2011;1(2):75-79.
  • [25] Vijayakumar PP, Muriana PM. A microplate growth inhibition assay for screening bacteriocins against Listeria monocytogenes to differentiate their mode-of-action. Biomolecules. 2015;5(2):1178-1194. https://doi.org/10.3390/biom5021178
  • [26] Boyanova L, Stephanova-Kondratenko M, Mitov I. Anti-Helicobacter pylori activity of Lactobacillus delbrueckii subsp. bulgaricus strains: preliminary report. J Appl Microbiol. 2008;48:579–584. https://doi.org/10.1111/j.1472-765X.2009.02571.x
  • [27] Mattana CM, Satorres SE, Sosa A, Fusco M, Alcaráz LE. Antibacterial activity of extracts of Acacia aroma against methicillin-resistant and methicillin-sensitive Staphylococcus. Brazilian J Microbiol. 2010;41(3):581-587. https://doi.org/10.1590/S1517-83822010000300007
  • [28] EUCAST (2015) Disc diffusion method for antimicrobial susceptibility testing issue. Version 5.0.

Yıl 2023, Cilt: 27 Sayı: 6, 2374 - 2388, 28.06.2025

Nurten Tetik Pervin Rayaman , Erkan Rayaman , Rıza Adaleti

Öz

Kaynakça

  • [1] Compare D, Sgamato C, Nardone OM, Rocco A, Coccoli P, Laurenza C, Nardone G. Probiotics in gastrointestinal diseases: All that glitters is not gold. Dig Dis. 2022;40(1):123-132. https://doi.org/10.1159/000516023.
  • [2] Ghannoum MA, McCormick TS, Retuerto M, Bebek G, Cousineau S, Hartman L, Barth C, Schrom K. Evaluation of microbiome alterations following consumption of BIOHM, a novel probiotic. Curr Issues Mol Biol. 2021;43(3):2135-2146. https://doi.org/10.3390/cimb43030148
  • [3] Hashim ZA. Evaluation of bacterial contents, package labelling and antimicrobial activity of some commercial probiotic products available in local market. J Res Pharm. 2022;26(3):502-509. http://dx.doi.org/10.29228/jrp.147
  • [4] Castellone V, Bancalari E, Rubert J, Gatti M, Neviani E, Bottari B. Eating fermented: Health benefits of LAB-fermented foods. Foods. 2021;10(11):26-39. https://doi.org/10.3390/foods10112639
  • [5] Ouwehand AC, Vesterlund S. Antimicrobial components from lactic acid bacteria. In: Salminen S, (ed). Lactic Acid Bacteria. 3rd edn. Marcel Dekker, New York, 2004, pp 375-397.
  • [6] Ong JS, Taylor TD, Yong CC, Khoo BY, Sasidharan S, Choi SB, Ohno H, Liong MT. Lactobacillus plantarum USM8613 aids in wound healing and suppresses Staphylococcus aureus infection at wound sites. Probiotics Antimicrob Proteins. 2020;12(1):125-137. https://doi.org/10.1007/s12602-018-9505-9
  • [7] Dinçer, E., Kıvanç, M. Invitro evaluation of probiotic potential of Enterococcus faecium strains isolated from Turkish pastırma. Archives of Microbiology. 2021;203(6), 2831-2841. https://doi.org/10.1007/s00203-021-02273-y.
  • [8] Yoha KS, Nida S, Dutta S, Moses JA, Anandharamakrishnan C. Targeted delivery of probiotics: perspectives on research and commercialization. Probiotics Antimicrob Proteins. 2021;27:1-34. https://doi.org/10.1007/s12602-021-09791-7
  • [9] Yılmaz M, Şeker E. Investigation of mecA, vanA and PVL genes in Staphylococcus aureus strains isolated from bovine mastitis in small holder dairy farms. Etlik Vet Mikrobiyol Derg. 2022;33(1):50-55. https://doi.org/10.35864/evmd.1008728
  • [10] Alışkan HE, Başustaoğlu A. Determination of biofilm formation properties of methicillin sensitive and resistant Staphylococcus aureus isolates by conventional and molecular methods. Mikrobiyoloji Bul. 2020;54(2):223-234. https://doi.org/10.5578/mb.69204
  • [11] Park S, Classen A, Gohou HM, Maldonado R, Kretschmann E, Duvernay C, Kim GK, Ronholm J. A new, reliable, and high-throughput strategy to screen bacteria for antagonistic activity against Staphylococcus aureus. BMC Microbiol. 2021;21(1):189. https://doi.org/10.1186/s12866-021-02265-4
  • [12] Mazzantini D, Celandroni F, Calvigioni M, Panattoni A, Labella R, Ghelardi E. Microbiological Quality and Resistance to an Artificial Gut Environment of Two Probiotic Formulations. Foods. 2021;10(11):2781. https://doi.org/10.3390/foods10112781
  • [13] Rolfe RD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr. 2000;130:396-402. https://doi.org/10.1093/jn/130.2.396S
  • [14] Çoşkun T. Probiotics. In: Kara A, Çoşkun T (eds) Prebiotics and probiotics from theory to clinic. Ömür Typography AC, İstanbul, 2014, pp:56-7.
  • [15] Durak Y, Uysal A, Aladağ MO, Akın D. Ticari yoğurt örneklerinden canlı laktik asit bakterilerinin izolasyonu ve sayımı (Isolation and counting of live lactic acid bacteria from commercial yogurt samples). SUFEFD. 2015;41:83-88.
  • [16] Dumani A, Yoldaş O, Akçimen B, Yılmaz Ş, Köksal F. Farklı çeşitteki Türk peynirlerinde Enterococcus faecalis türünün tespiti. Atatürk Üniv Diş Hek Fak Derg. 2015;25(1):35-9. https://doi.org/10.17567/dfd.97125
  • [17] Tomar O, Çağlar A, Akarca G. Kefir ve sağlık açısından önemi. AKÜ FEMÜBİD. 2017;17(2):834-853. https://doi.org/10.5578/fmbd.57533
  • [18] Çelikel A, Göncü B, Akın MB, Akın MS. Süt ürünlerinde probiyotik bakterilerin canlılığını etkileyen faktörler. Batman Üniversitesi Yaşam Bilimleri Dergisi. 2018;8(1/2):59-68.
  • [19] Schillinger U, Lucke FK. Antibacterial activity of Lactobacillus sakei isolated from meat. Appl Environ Microbiol. 1989;5(8):1901-1906. https://doi.org/10.1128/aem.55.8.1901-1906.1989
  • [20] Özdemir H, Küplülü Ö, Çelik HT. Determination of antibacterial effects of Lactobacilli isolated from Turkish Fermented Sausage. Gıda. 2002;27(6):539-544.
  • [21] Tuncer Y, Özden B, Akçelik M. Lactococcus lactis subsp. from tulum cheese partial characterization of bacteriocins produced by lactis YBML9 and YBML21 strains. SDÜ Fen Bil Enst Der. 2008;12(2):141-148.
  • [22] Goderska K, Czarnecki Z. Characterization of selected strains from Lactobacillus acidophilus and Bifidobacterium bifidum. Afr J Microbiol Res. 2007;1(6):65-78.
  • [23] Altuntaş EG, Ayhan K, Okcu G, Erkanlı K, Balcı MH, Sonakın ŞS. Antimicrobial activities of lactic acid bacteria isolated from raw milk and cheese samples. Gıda. 2010;35(3):197-203.
  • [24] Hassan M, Javadzadeh Y, Lotfipour F, Badomchi R. Determination of comparative minimum inhibitory concentration (MIC) of bacteriocins produced by enterococci for selected isolates of multi-antibiotic resistant Enterococcus spp. Adv Pharm Bull. 2011;1(2):75-79.
  • [25] Vijayakumar PP, Muriana PM. A microplate growth inhibition assay for screening bacteriocins against Listeria monocytogenes to differentiate their mode-of-action. Biomolecules. 2015;5(2):1178-1194. https://doi.org/10.3390/biom5021178
  • [26] Boyanova L, Stephanova-Kondratenko M, Mitov I. Anti-Helicobacter pylori activity of Lactobacillus delbrueckii subsp. bulgaricus strains: preliminary report. J Appl Microbiol. 2008;48:579–584. https://doi.org/10.1111/j.1472-765X.2009.02571.x
  • [27] Mattana CM, Satorres SE, Sosa A, Fusco M, Alcaráz LE. Antibacterial activity of extracts of Acacia aroma against methicillin-resistant and methicillin-sensitive Staphylococcus. Brazilian J Microbiol. 2010;41(3):581-587. https://doi.org/10.1590/S1517-83822010000300007
  • [28] EUCAST (2015) Disc diffusion method for antimicrobial susceptibility testing issue. Version 5.0.
Toplam 28 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Eczacılık ve İlaç Bilimleri (Diğer)
Bölüm Articles
Yazarlar

Nurten Tetik

Pervin Rayaman 0000-0002-0487-8692

Erkan Rayaman 0000-0002-1261-3942

Rıza Adaleti 0000-0001-9576-6794

Yayımlanma Tarihi 28 Haziran 2025
Yayımlandığı Sayı Yıl 2023 Cilt: 27 Sayı: 6

Kaynak Göster

APA Tetik, N., Rayaman, P., Rayaman, E., Adaleti, R. (2025). Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates. Journal of Research in Pharmacy, 27(6), 2374-2388.
AMA Tetik N, Rayaman P, Rayaman E, Adaleti R. Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates. J. Res. Pharm. Temmuz 2025;27(6):2374-2388.
Chicago Tetik, Nurten, Pervin Rayaman, Erkan Rayaman, ve Rıza Adaleti. “Antimicrobial Effect of Probiotic Microorganisms on Clinical and Standard Staphylococcus Aureus Isolates”. Journal of Research in Pharmacy 27, sy. 6 (Temmuz 2025): 2374-88.
EndNote Tetik N, Rayaman P, Rayaman E, Adaleti R (01 Temmuz 2025) Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates. Journal of Research in Pharmacy 27 6 2374–2388.
IEEE N. Tetik, P. Rayaman, E. Rayaman, ve R. Adaleti, “Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates”, J. Res. Pharm., c. 27, sy. 6, ss. 2374–2388, 2025.
ISNAD Tetik, Nurten vd. “Antimicrobial Effect of Probiotic Microorganisms on Clinical and Standard Staphylococcus Aureus Isolates”. Journal of Research in Pharmacy 27/6 (Temmuz 2025), 2374-2388.
JAMA Tetik N, Rayaman P, Rayaman E, Adaleti R. Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates. J. Res. Pharm. 2025;27:2374–2388.
MLA Tetik, Nurten vd. “Antimicrobial Effect of Probiotic Microorganisms on Clinical and Standard Staphylococcus Aureus Isolates”. Journal of Research in Pharmacy, c. 27, sy. 6, 2025, ss. 2374-88.
Vancouver Tetik N, Rayaman P, Rayaman E, Adaleti R. Antimicrobial effect of probiotic microorganisms on clinical and standard Staphylococcus aureus isolates. J. Res. Pharm. 2025;27(6):2374-88.