Evaluation of anti-biofilm activity of Lactobacillus rhamnosus GG and Nisin on the expression of aap, ica-A and ica-D as biofilm-associated genes of Staphylococcus epidermidis
-
Mohammad Dalvand
,
Seyed Ali Mirhosseini
,
Kiumarss Amini
,
Soghra Khani
,
Hamideh Mahmoodzadeh Hosseini
,
Kowsar Mansoori
Abstract
Background and Objectives: In the present study, the anti-biofilm activity of Lactobacillus rhamnosus GG and Nisin was investigated on biofilm-forming abilities of Staphylococcus epidermidis strains and the expression of the biofilm-associated genes.
Materials and Methods: In this study, the standard strain of L. rhamnosus GG (ATCC 53103) and Nisin were used to assess their anti-microbial and anti-biofilm effects on S. epidermidis (RP62A).
Results: The MIC and MBC analysis showed that Nisin at 256 μg/mL and 512 μg/mL, and L. rhamnosus GG at 1×107 CFU/mL and 1×108 CFU/mL have anti-microbial activity compared to the negative control respectively. L. rhamnosus GG bacteria and Nisin inhibited the biofilm formation of S. epidermidis based on optical density of at 570 nm (P <0.001). The relative mRNA expression of aap, icaA, and icaD genes was significantly reduced compared to the negative control after treating S. epidermidis with sub-MIC of Nisin (0.44, 0.25 and 0.6 fold, respectively) (P>0.05). In addition, the relative expression of aap and icaA genes, but not icaD (P>0.05), was significantly lower than the negative control (0.62 and 0.7 fold, respectively) (P>0.05), after exposure to the sub MIC of L. rhamnosus GG.
Conclusion: Nisin and L. rhamnosus GG exhibit potent activity against biofilm-forming abilities of S. epidermidis and these agents could be utilized as an anti-biofilm agents against S. epidermidis infections.
1. Namvar AE, Bastarahang S, Abbasi N, Ghehi GS, Farhadbakhtiarian S, Arezi P, et al. Clinical characteristics of Staphylococcus epidermidis: a systematic review. GMS Hyg Infect Control 2014; 9: Doc23.
2. Skovdal M, Khayinza Sorensen ON, Muchemwa D, Nyamwanza RP, Maswera R, Svendsen MN, et al. "It will not be easy to accept": Parents conflicting attitudes towards pre-exposure prophylaxis for HIV prevention amongst adolescent girls and young women. Res Social Adm Pharm 2023; 19: 266-271.
3. Lou Q, Zhu T, Hu J, Ben H, Yang J, Yu F, et al. Role of the SaeRS two-component regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. BMC Microbiol 2011; 11: 146.
4. Kant R, Rintahaka J, Yu X, Sigvart-Mattila P, Paulin L, Mecklin JP, et al. A comparative pan-genome perspective of niche-adaptable cell-surface protein phenotypes in Lactobacillus rhamnosus. PLoS One 2014; 9(7): e102762.
5. Mathipa-Mdakane MG, Thantsha MS. Lacticaseibacillus rhamnosus: a suitable Candidate for the construction of novel bioengineered probiotic strains for targeted pathogen control. Foods 2022; 11: 785.
6. Segers ME, Lebeer S. Towards a better understanding of Lactobacillus rhamnosus GG--host interactions. Microb Cell Fact 2014; 13 Suppl 1(Suppl 1): S7.
7. Doron S, Snydman DR, Gorbach SL. Lactobacillus GG: bacteriology and clinical applications. Gastroenterol Clin North Am 2005; 34: 483-98, ix.
8. Martin R, Chamignon C, Mhedbi-Hajri N, Chain F, Derrien M, Escribano-Vazquez U, et al. The potential probiotic Lactobacillus rhamnosus CNCM I-3690 strain protects the intestinal barrier by stimulating both mucus production and cytoprotective response. Sci Rep 2019; 9: 5398.
9. Spacova I, O'Neill C, Lebeer S. Lacticaseibacillus rhamnosus GG inhibits infection of human keratinocytes by Staphylococcus aureus through mechanisms involving cell surface molecules and pH reduction. Benef Microbes 2020; 11: 703-715.
10. Szajewska H, Wanke M, Patro B. Meta-analysis: the effects of Lactobacillus rhamnosus GG supplementation for the prevention of healthcare-associated diarrhoea in children. Aliment Pharmacol Ther 2011; 34: 1079-1087.
11. Yun B, Ryu S, Kang M, Lee J, Yoo J, Kim Y, et al. Probiotic Lacticaseibacillus rhamnosus GG increased longevity and resistance against foodborne pathogens in Caenorhabditis elegans by regulating MicroRNA miR-34. Front Cell Infect Microbiol 2022; 11: 819328.
12. Slykerman RF, Hood F, Wickens K, Thompson JMD, Barthow C, Murphy R, et al. Effect of Lactobacillus rhamnosus HN001 in pregnancy on postpartum symptoms of depression and anxiety: a randomised double-blind placebo-controlled trial. EBioMedicine 2017; 24: 159-165.
13. Boonma P, Spinler JK, Venable SF, Versalovic J, Tumwasorn S. Lactobacillus rhamnosus L34 and Lactobacillus casei L39 suppress Clostridium difficile-induced IL-8 production by colonic epithelial cells. BMC Microbiol 2014; 14: 177.
14. Liu J, Huang R, Song Q, Xiong H, Ma J, Xia R, et al. Combinational antibacterial activity of Nisin and 3-Phenyllactic acid and their co-production by engineered Lactococcus lactis. Front Bioeng Biotechnol 2021; 9: 612105.
15. de Arauz LJ, Jozala AF, Mazzola PG, Penna TCV. Nisin biotechnological production and application: a review. Trends Food Sci Tech 2009; 20: 146-154.
16. Shin JM, Gwak JW, Kamarajan P, Fenno JC, Rickard AH, Kapila YL. Biomedical applications of nisin. J Appl Microbiol 2016; 120: 1449-1465.
17. Barbosa AAT, Mantovani HC, Jain S. Bacteriocins from lactic acid bacteria and their potential in the preservation of fruit products. Crit Rev Biotechnol 2017; 37: 852-864.
18. Ceotto-Vigoder H, Marques SLS, Santos INS, Alves MDB, Barrias ES, Potter A, et al. Nisin and lysostaphin activity against preformed biofilm of Staphylococcus aureus involved in bovine mastitis. J Appl Microbiol 2016; 121: 101-114.
19. Field D, O'Connor R, Cotter PD, Ross RP, Hill C. In vitro activities of Nisin and Nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Front Microbiol 2016; 7: 508.
20. Mottaghiyan Z, Aghazadeh M, Hosseini HM, Fooladi AAI. Evaluation of antibacterial activity of Zataria multiflora against the expression of icaADB and aap Gene and biofilm formation in Staphylococcus epidermidis. Arch Clin Infect Dis 2019; 14: e65321.
21. Merritt JH, Kadouri DE, O'Toole GA. Growing and analyzing static biofilms. Curr Protoc Microbiol 2005; Chapter 1:Unit 1B.1.
22. Pintens V, Massonet C, Merckx R, Vandecasteele S, Peetermans WE, Knobloch JK, et al. The role of sigmaB in persistence of Staphylococcus epidermidis foreign body infection. Microbiology (Reading) 2008; 154: 2827-2836.
23. Twomey E, Hill C, Field D, Begley M. Bioengineered Nisin derivative M17Q has enhanced activity against Staphylococcus epidermidis. Antibiotics (Basel) 2020; 9: 305.
24. Pimentel-Filho Nde J, Martins MC, Nogueira GB, Mantovani HC, Vanetti MC. Bovicin HC5 and nisin reduce Staphylococcus aureus adhesion to polystyrene and change the hydrophobicity profile and Gibbs free energy of adhesion. Int J Food Microbiol 2014; 190: 1-8.
25. Mahdavi M, Jalali M, Kermanshahi RK. The effect of nisin on biofilm forming foodborne bacteria using microtiter plate method. Res Pharma Sci 2009; 2: 113-118.
26. Saidi N, Saderi H, Owlia P, Soleimani M. Anti-biofilm potential of Lactobacillus casei and Lactobacillus rhamnosus cell-free supernatant extracts against Staphylococcus aureus. Adv Biomed Res 2023; 12: 50.
27. Soderling EM, Marttinen AM, Haukioja AL. Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol 2011; 62: 618-622.
28. Lee S-H, Kim Y-J. A comparative study of the effect of probiotics on cariogenic biofilm model for preventing dental caries. Arch Microbiol 2014; 196: 601-609.
29. Petrova MI, Imholz NC, Verhoeven TL, Balzarini J, Van Damme EJ, Schols D, et al. Lectin-like molecules of Lactobacillus rhamnosus GG inhibit pathogenic Escherichia coli and Salmonella biofilm formation. PLoS One 2016; 11(8): e0161337.
2. Skovdal M, Khayinza Sorensen ON, Muchemwa D, Nyamwanza RP, Maswera R, Svendsen MN, et al. "It will not be easy to accept": Parents conflicting attitudes towards pre-exposure prophylaxis for HIV prevention amongst adolescent girls and young women. Res Social Adm Pharm 2023; 19: 266-271.
3. Lou Q, Zhu T, Hu J, Ben H, Yang J, Yu F, et al. Role of the SaeRS two-component regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. BMC Microbiol 2011; 11: 146.
4. Kant R, Rintahaka J, Yu X, Sigvart-Mattila P, Paulin L, Mecklin JP, et al. A comparative pan-genome perspective of niche-adaptable cell-surface protein phenotypes in Lactobacillus rhamnosus. PLoS One 2014; 9(7): e102762.
5. Mathipa-Mdakane MG, Thantsha MS. Lacticaseibacillus rhamnosus: a suitable Candidate for the construction of novel bioengineered probiotic strains for targeted pathogen control. Foods 2022; 11: 785.
6. Segers ME, Lebeer S. Towards a better understanding of Lactobacillus rhamnosus GG--host interactions. Microb Cell Fact 2014; 13 Suppl 1(Suppl 1): S7.
7. Doron S, Snydman DR, Gorbach SL. Lactobacillus GG: bacteriology and clinical applications. Gastroenterol Clin North Am 2005; 34: 483-98, ix.
8. Martin R, Chamignon C, Mhedbi-Hajri N, Chain F, Derrien M, Escribano-Vazquez U, et al. The potential probiotic Lactobacillus rhamnosus CNCM I-3690 strain protects the intestinal barrier by stimulating both mucus production and cytoprotective response. Sci Rep 2019; 9: 5398.
9. Spacova I, O'Neill C, Lebeer S. Lacticaseibacillus rhamnosus GG inhibits infection of human keratinocytes by Staphylococcus aureus through mechanisms involving cell surface molecules and pH reduction. Benef Microbes 2020; 11: 703-715.
10. Szajewska H, Wanke M, Patro B. Meta-analysis: the effects of Lactobacillus rhamnosus GG supplementation for the prevention of healthcare-associated diarrhoea in children. Aliment Pharmacol Ther 2011; 34: 1079-1087.
11. Yun B, Ryu S, Kang M, Lee J, Yoo J, Kim Y, et al. Probiotic Lacticaseibacillus rhamnosus GG increased longevity and resistance against foodborne pathogens in Caenorhabditis elegans by regulating MicroRNA miR-34. Front Cell Infect Microbiol 2022; 11: 819328.
12. Slykerman RF, Hood F, Wickens K, Thompson JMD, Barthow C, Murphy R, et al. Effect of Lactobacillus rhamnosus HN001 in pregnancy on postpartum symptoms of depression and anxiety: a randomised double-blind placebo-controlled trial. EBioMedicine 2017; 24: 159-165.
13. Boonma P, Spinler JK, Venable SF, Versalovic J, Tumwasorn S. Lactobacillus rhamnosus L34 and Lactobacillus casei L39 suppress Clostridium difficile-induced IL-8 production by colonic epithelial cells. BMC Microbiol 2014; 14: 177.
14. Liu J, Huang R, Song Q, Xiong H, Ma J, Xia R, et al. Combinational antibacterial activity of Nisin and 3-Phenyllactic acid and their co-production by engineered Lactococcus lactis. Front Bioeng Biotechnol 2021; 9: 612105.
15. de Arauz LJ, Jozala AF, Mazzola PG, Penna TCV. Nisin biotechnological production and application: a review. Trends Food Sci Tech 2009; 20: 146-154.
16. Shin JM, Gwak JW, Kamarajan P, Fenno JC, Rickard AH, Kapila YL. Biomedical applications of nisin. J Appl Microbiol 2016; 120: 1449-1465.
17. Barbosa AAT, Mantovani HC, Jain S. Bacteriocins from lactic acid bacteria and their potential in the preservation of fruit products. Crit Rev Biotechnol 2017; 37: 852-864.
18. Ceotto-Vigoder H, Marques SLS, Santos INS, Alves MDB, Barrias ES, Potter A, et al. Nisin and lysostaphin activity against preformed biofilm of Staphylococcus aureus involved in bovine mastitis. J Appl Microbiol 2016; 121: 101-114.
19. Field D, O'Connor R, Cotter PD, Ross RP, Hill C. In vitro activities of Nisin and Nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Front Microbiol 2016; 7: 508.
20. Mottaghiyan Z, Aghazadeh M, Hosseini HM, Fooladi AAI. Evaluation of antibacterial activity of Zataria multiflora against the expression of icaADB and aap Gene and biofilm formation in Staphylococcus epidermidis. Arch Clin Infect Dis 2019; 14: e65321.
21. Merritt JH, Kadouri DE, O'Toole GA. Growing and analyzing static biofilms. Curr Protoc Microbiol 2005; Chapter 1:Unit 1B.1.
22. Pintens V, Massonet C, Merckx R, Vandecasteele S, Peetermans WE, Knobloch JK, et al. The role of sigmaB in persistence of Staphylococcus epidermidis foreign body infection. Microbiology (Reading) 2008; 154: 2827-2836.
23. Twomey E, Hill C, Field D, Begley M. Bioengineered Nisin derivative M17Q has enhanced activity against Staphylococcus epidermidis. Antibiotics (Basel) 2020; 9: 305.
24. Pimentel-Filho Nde J, Martins MC, Nogueira GB, Mantovani HC, Vanetti MC. Bovicin HC5 and nisin reduce Staphylococcus aureus adhesion to polystyrene and change the hydrophobicity profile and Gibbs free energy of adhesion. Int J Food Microbiol 2014; 190: 1-8.
25. Mahdavi M, Jalali M, Kermanshahi RK. The effect of nisin on biofilm forming foodborne bacteria using microtiter plate method. Res Pharma Sci 2009; 2: 113-118.
26. Saidi N, Saderi H, Owlia P, Soleimani M. Anti-biofilm potential of Lactobacillus casei and Lactobacillus rhamnosus cell-free supernatant extracts against Staphylococcus aureus. Adv Biomed Res 2023; 12: 50.
27. Soderling EM, Marttinen AM, Haukioja AL. Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol 2011; 62: 618-622.
28. Lee S-H, Kim Y-J. A comparative study of the effect of probiotics on cariogenic biofilm model for preventing dental caries. Arch Microbiol 2014; 196: 601-609.
29. Petrova MI, Imholz NC, Verhoeven TL, Balzarini J, Van Damme EJ, Schols D, et al. Lectin-like molecules of Lactobacillus rhamnosus GG inhibit pathogenic Escherichia coli and Salmonella biofilm formation. PLoS One 2016; 11(8): e0161337.
| Files | ||
| Issue | Vol 15 No 4 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i4.13509 | |
| Keywords | ||
| Staphylococcus epidermidis; Probiotic; Lactobacillus rhamnosus GG; Nisin; Biofilm | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Dalvand M, Mirhosseini SA, Amini K, Khani S, Mahmoodzadeh Hosseini H, Mansoori K. Evaluation of anti-biofilm activity of Lactobacillus rhamnosus GG and Nisin on the expression of aap, ica-A and ica-D as biofilm-associated genes of Staphylococcus epidermidis. Iran J Microbiol. 2023;15(4):550-556.
