Comparison between Antimicrobial and Antibiofilm Activity of Exopolysaccharides (EPS) Extracted from Lactobacillus reuteri and Streptococcus mitis against Oral Bacteria

Document Type : Original Articles

Authors

1 Department of Medical Laboratories, College of Medical and Health Techniques, Sawa University, Samawah, Iraq

2 College of Veterinary Medicine, Al-Muthanna University, Samawah, Iraq

Abstract

Due to the increased resistance to antibiotics and chemical biocides, the use of bacterial exopolysaccharides has been considered. The objective of the current study was to investigate the strength of the antibacterial and antibiofilm activity of EPS extracted from Lactobacillus reuteri and Streptococcus mitis because previous studies showed there were structural differences between EPS, during this study, EPS extracted from Lactobacillus reuteri and Streptococcus miti by ethanol precipitation method and estimated antibacterial and antibiofilm activity against several Oral Bacteria (Staphylococcus aureus, Staphylococcus hominis, Acinetobacter baumannii, Raoultella ornithinolytica, Streptococcus thoraltensis in different concentration as (100,150,200,250,300 mg/ml ), the results showed carbohydrates rate in extracted  EPS from L. reuteri  and S. mitis were recorded was 85, 80 % respectively.The concentration 100 and 150 mg/ml for EPS from L. reuteri  and S. mitis, there was no inhibitory effect, except in S. aureus (1.1±0.10)  and S. hominis (1.0±0.10) at 100 mg/ml, 3.1±2.01, 2.1±0.54 mg/ml respectively at 150 mg/ml concentration but no significant differences (P≤0.05). However, the antibacterial effect of that EPSs started at the concentration of 200 and upwards, where different results were recorded between the concentrations of both EPSs against all bacteria isolated (P≤0.05), On the other hand, the effect of EPS from L. reuteri  and S. mitis was clear against the formation of biofilm compared with the control, worth mentioning that EPS from L. reuteri was more effective compared with EPS from S. mitis in all isolates (P≤0.05) except for S. thoraltensis where it was noted that the EPS from S. mitis is more effective than EPS from L. reuteri. Through the results obtained in this study, it was noted that the difference in the structural nature of EPS has an important role in its effectiveness as an antibacterial and anti-biofilm formation and, as it was found that the EPS from L. reuteri showed more effectiveness than EPS from S. mitis and thus the mechanism of preventing and inhibiting bacteria depending of the structural nature of EPS.

Keywords

1. Introduction

Microbial polysaccharides have various properties, and they are used as drug delivery agents, bio-absorbents and bio-flocculants in the food, pharmaceutical industries and cosmetics ( 1 , 2 ). Polysaccharides are employed in green manufacturing of silver nanoparticles because they are more beneficial than synthetic polymers ( 3 ).

The interaction of metal ions with hydroxyl groups of EPS significantly impacts the form and size of nanoparticles ( 4 ) and found that EPS is biodegradable, non-toxic, biocompatible, and plentiful in natural sources. Enterococcus sp., Bifidobacterium sp., Lactococcus sp., Pediococcus sp., Leuconostoc sp., Streptococcus sp., Lactobacillus sp. and Weissella sp. are the most common EPS producers ( 5 ). Among the many microorganisms consumed by humans, Probiotic bacteria survive in bile presence, gastric secretions, and low pH and colonize the gastrointestinal tract ( 6 , 7 ). Antibiotic use decreases the antagonistic activity of normal microbial flora against pathogenic germs ( 8 ).

Probiotics can counteract antibiotics, which can cause immunological suppression if consumed regularly. They strengthen the immune system to suppress diseases caused by pathogen microorganisms ( 9 ). As a result, probiotic Exopolysaccharides (EPS) are used to treat autoimmune diseases, inflammatory gastrointestinal diseases, colon cancer, gastric ulcers, cardiovascular diseases, and obesity in humans ( 10 ).

Biological roles and functional features of bacterial EPSare influenced by their chemical structures, which are diverse and complex. They are classified as hemopolysaccharides (HoPS) or heteropolysaccharides (HePS), which contain two or more monosaccharides. Most of the EPS produced by LAB is HePS, which is produced intracellularly, but other LAB species/strains created EPS as (HoPS) via external enzymes ( 11 ). HoPS generated by LAB can be classed as fructans, glucans, or galactans; they contain D-galactose, D-fructose D-glucose ( 12 ).

Hemopolysaccharides have a more complex structure as they are composed of several repeating units of sugars, such as hexose, pentose, uronic acids or N-acetylated monosaccharides and may be branched or unbranched ( 13 ). The present study investigated the antimicrobial and antibiotic activity of exopolysaccharides (EPS) extracted from Lactobacillus ruteri and Streptococcus mitis against oral bacteria.

2. Materials and Methods

2.1. Bacteria Isolated from the Oral Cavity.

The isolated (S. aureus, S. hominis, A. baumannii, R. ornithinolytica and S. thoraltensis) obtained from the department of Microbiology and Parasitology, college of veterinary medicine, which was isolated from the oral cavity of some animals such as camels and cows and confirmed with Vitek system.

2.2. Purification and Extraction EPSs.

EPSs are extracted using ethanol precipitation ( 14 ). L. reuteri was grown in MRS broth for 24 hours, whereas S. Mitis was cultivated in brain heart broth for 24 hours. After centrifuging at 8,000 g for 20 min at 40C, the supernatant was collected and denatured with a trichloroacetic acid (final concentration of 14 %). The supernatant was added to absolute cold ethanol (two-fold volume of supernatant) and kept at 4C° for 24 hours before being centrifuged at 8000g for 20 minutes. The supernatant was removed after centrifuging the precipitated exopolysaccharide for 15 minutes at 4C°. Finally, the precipitate was dissolved in deionized water and dialyzed for 24 to 48 hours using a dialysis membrane. The precipitated exopolysaccharides dried at 30C° to remove the ethanol before being concentrated, and carbohydrate content was determined using the phenol-sulfuric-acid technique.

2.3. Determination MIC of EPSs

In Eppendorf tubes, 100 µl of bacterial suspension (adjusted to 0.5 McFarland standard) was added, followed by 50 µl of EPSs, and the tubes were incubated for 24 hr. at 37 C°. The tubes were then checked for turbidity, with the tubes that exhibited turbidity being excluded and those that did not show turbidity being recognized as the minimal inhibitory concentration ( 15 ).

2.4. Determination of the Antibiotic Activity of EPSs

Isolates were activated in nutrient broth (18 to 24 h) and then corrected to a McFarland standard even to 1.5 × 108 CFU/ml) then subculture on Mueller-Hinton agar followed by creating equal-sized (6 mm diameter) to fill up with 0.1 ml of prepared concentration of EPS ( 15 ).

2.5. MIC Effects of EPSs on Preformed Biofilm

The wells were filled with 100 μl of tryptic soy broth (TSB) cultured bacteria (96-well plate), then incubated at 37°C for 24 h biofilm formation; the medium was generously aspirated while formed biofilm was washed three times with PBS to remove non-adherent cells; finally, 200 μl of EPS in TSB was added to the well and incubated for 24 hr. at 37C°, and the experiment was performed without the MIC of EPS as a control ( 16 ).

2.6. Statistical Analysis

All data collected using Microsoft Excel 2016 and SPSS version 18 to assess the significance of the observed differences between the treatments used were subjected to analysis of variance (ANOVA), and Fisher's least significant difference (LSD) (P<0.05) was measured statistically significant.

3. Results and Discussion

The results of the determination of carbohydrates rate in purified EPS from L. reuteri and S. mitis were recorded the carbohydrate content was 85, and 80%, respectively, by using the phenol-sulfuric-acid-method while the 15-20% other components, such as acetyl group, Ketal Linked pyruvate, group, Hexominase and uronic acids ( 17 ). TCA was used to denature protein components during the extraction process ( 14 ), which according to the study of Dilna, Surya ( 18 ), in the extraction of exopolysaccharides from long-chain molecules consisting of sugar and/or sugar derivatives, but rhamnose, galactose, glucose were obtained ( 19 ). EPS showed the highest proportion of carbohydrates.

The results of the MIC activity recorded that EPS from L. reuteri at 50 mg and S. mitis at 60 mg was able to inhibit the growth of S. aureus, but the study recorded that high concentrations of EPS from L. reuteri and S. mitis at 85 mg, 76 mg respectively required to inhibit R. ornithinolytica as well as 162 mg, 170 mg respectively required to inhibit S. thoraltensis as in figure 1.

Figure 1. MIC activity of EPS of L. reuteri and S. mitis against bacteria isolated from the oral cavity

When using the concentrations 100 and 150 mg/ml for EPS from L. reuteri and S. mitis, there was no inhibitory effect on the isolates used in the study, except in S. aureus and S. hominis which both EPS from L. reuteri and S. mitis recorded 1.1±0.10 against S. aureus and 1.0±0.10 against S. hominis at 100 mg/ml while at 150 mg/ml against S. aureus 3.1±2.01, S. hominis 2.1±0.54 mg/ml but no significant differences between concentrations of EPS (P≤0.05), however, the antibacterial effect of that EPSs started at the concentration of 200 and upwards, where different results were recorded between the concentrations of both EPSs against all isolate with the presence of significant differences (P≤0.05), in addition, the study showed that the antibacterial effect of EPS from L. reuteri was higher compared to the antibacterial effect of EPS from S. mitis depending on the area of inhibition as in the figures 2, 3, 4, 5 and 6 and table 1.

Figure 2. Antibacterial activity of EPSs in concentration 100 mg/ml

Figure 3. Antibacterial activity of EPSs in concentration 150 mg/ml

Figure 4. The antibacterial activity of EPSs in a concentration of 200 mg/ml

Figure 5. Antibacterial activity of EPSs in concentration 250 mg/ml

Figure 6. Antibacterial activity of EPSs in concentration 300 mg/ml

Isolates EPS 100 mg/ml 150 mg/ml 200 mg/ml 250 mg/ml 300 mg/ml
S. aureus EPS 1 1.1±0.10a 3.1±2.01a 4.2±0.62a 6.2±0.76a 8.1±0.11a
EPS 2 1±0.02a 2.1±0.02b 3.2±0.12b 4.2±1.02b 6.2±0.02b
S. hominis EPS 1 1.0±0.00a 2.1±0.54a 3.3±0.32a 5.5±0.80a 7.1±0.02a
EPS 2 0±0.00a 1±0.02a 2.1±0.41b 3.1±0.52b 6.0±0.00b
A. baumannii EPS 1 0±0.00a 0±0.00a 1.1±0.23a 3.2±0.92a 4.4±0.32a
EPS 2 0±0.00a 0±0.00a 1.0±0.25a 1.0±0.00b 2.0±0.00b
R. ornithinolytica EPS 1 0±0.00a 0±0.00a 1.2±1.02a 3.33±1.92a 5.1±0.12a
EPS 2 0±0.00a 0±0.00a 1.1±0.20a 2.3±2.32b 3.5±0.30b
S. thoraltensis EPS 1 0±0.00a 1±0.00a 3.0±1.20a 4.3±2.82a 5.4±0.58a
EPS 2 0±0.00a 0±0.00a 1.0±0.00b 1.2±1.12b 3.0±0.00b
EPS1: EPS from L.reuteri, EPS2: EPS from S. mitis. The different letter means there was a significant difference between P≤0.05, the similar letters mean there was no significant difference between P≤ 0.05
 Table 1.Comparison of antibacterial activity of EPSs in different concentration (mg/ml) depending inhibition diameter zone (mm) by using T test (Mean±S.D)

The antibacterial activity of EPS in the current results are consistent with various studies ( 20 - 22 ); EPS obtained in LAB has a significant antibacterial effect. Gram-negative and positive bacteria. The EPS generated by L. rhamnosus showed significant antibacterial activity against the pathogens E. Coli and S. enterica ( 23 ).

Bacillus cereus, V. parahaemolyticus, S. Typhimurium, S. aureus and B. longum were affected by EPS produced by Bifidobacterium longum ( 24 ). EPS from L. gasseri was found to have antibacterial action against various pathogens, including Listeria monocytogenes, which was significantly suppressed in another study ( 25 ). When tested against E. coli and S. aureus, the EPS-C70 generated by L. Plantarum C70 isolated from camel milk resulted in a 2–3 log reduction in viability ( 26 ).

Although there is currently no clear mechanism for the antibacterial activity of EPS LAB against gram-positive and gram-negative bacteria, research is ongoing to establish an acceptable mechanism (s) for the antibacterial activity found. Since EPS has the potential to change the structure of bacterial cell coat, especially the peptidoglycan layer, it has been proposed as a suitable inhibitory mechanism ( 27 ).

The capacity of EPSs such as kefiran that interacts with the bacterial or eukaryotic cells led to the theory that kefiran acts as masking or decoy ( 28 ), this action may disrupt Gram-negative bacteria's outer membrane receptors or channels. Based on the study of Salachna, Mizielinska ( 29 ), the formation of secondary metabolites in the growth medium may be aided by EPS, which can damage bacteria. The antibacterial action of EPS is attributed to the functional groups in EPS structure interacting with bacterial cell envelopes ( 30 ). On the other hand, the effect of EPS from L. reuteri and S. mitis was clear against the formation of biofilm compared with the control; worth mentioning that EPS from L. reuteri was more effective compared with EPS from S. mitis in all isolates with the presence of significant differences except for S. thoraltensis isolates where it was noted that the EPS from S. mitis is more effective than EPS from L. reuteri 0.119±1.38, 0.150±0.40 respectively as in figure 7 and table 2.

Figure 7. Antibiofilm activity of EPSs EPSsagainst bacteria isolated from the oral cavit

Isolates Control EPS from Lac EPS from Strep
S. aureus 0.159±2.12a 0.133±0.02c 0.140±1.02b
S. hominis 0.153±1.02a 0.128±0.11c 0.172±0.98b
Abaumannii 0.165±0.32a 0.121±0.87c 0.132±0.90b
Rornithinolytica 0.107±0.44a 0.103±0.42b 0.104±0.35b
S.thoraltensis 0.166±0.65a 0.150±0.40b 0.119±1.38c
The different letter means there was a significant difference between P≤0.05 and the similar letters mean there was no significant difference between P≤0.05
 Table 2.Comparison of Antibiofilm activity of EPSs against bacteria isolated from the oral cavity

The antibiofilm results were consistent with ( 31 - 33 ). LAB's polysaccharides have anti-biofilm, immunostimulatory, and antioxidant properties ( 34 ). The findings revealed that the ability to remove biofilms is linked to the concentration of EPS ( 35 ). It is not understood how probiotics reduce biofilm development. Furthermore, EPS produced by L. acidophilus significantly reduced the expression of genes involved in chemotaxis and curli formation in E. coli, inhibiting biofilm development ( 36 ). These probiotics affect the expression of various C. albicans genes, such as ALS3, HWP1, EFG1 and SAP5. According to the findings, these probiotics were found to be efficient in suppressing biofilm formation and eliminating preformed biofilms of C. albicans ( 37 ). Because of the chemical structure of EPS, there are differences in antibacterial activity between EPS from L. reuteri and S. mitis. Exopolysaccharides (EPSs) are carbohydrate polymers with a high molecular weight that are released into the extracellular matrix by various bacteria. Based on their monosaccharide compositions, EPSs are divided into two groups homo-exopolysaccharides, made up of only one type of sugar with repeating subunits. Hetero-exopolysaccharides, are made up of two or more types of monosaccharide subunits ( 23 ). Medium ingredients and cultural circumstances all influence their structure and qualities. Furthermore, because of their molecular weights and functional groups' glycosidic linkages, their functional and rheological properties vary among industries ( 38 ).

4. Conclusion

The results obtained in this study was noted that the difference in the structural nature of EPS has a vital role in its effectiveness as an antibacterial and anti-biofilm formation, as it was found that the EPS from L. reuteri showed more effective than EPS from S. mitis and thus the mechanism of preventing and inhibiting bacteria depending of the structural nature of EPS, at the same time the results showed that some bacteria were resistant to both extracts depending on the radius of the inhibition zone at EPSs concentration lower than 200mg/ml but the antibacterial activity of both EPS was apparent at a concentration higher than 200 mg/ml.

Authors' Contribution

Study concept and design: S. M. A. and H. J. J.

Acquisition of data: H. J. J.

Analysis and interpretation of data: G. H. H.

Drafting of the manuscript: M. M. M. A.

Critical revision of the manuscript for important intellectual content: S. M. A. and H. J. J.

Statistical analysis: S. M. A.

Administrative, technical, and material support: H. J. J.

Ethics

In the present study, all ethical standards were approved by the Sawa University, Samawah, Iraq ethics committee.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Chen Z, Shi J, Yang X, Liu Y, Nan B, Wang Z. Isolation of exopolysaccharide-producing bacteria and yeasts from Tibetan kefir and characterisation of the exopolysaccharides. Int J Dairy Technol. 2016; 69:n/a-n/a.
  2. Silva LA, Lopes Neto JHP, Cardarelli HR. Exopolysaccharides produced by Lactobacillus plantarum: technological properties, biological activity, and potential application in the food industry. Ann Microbiol. 2019; 69(4):321-8.
  3. Kanmani P, Lim ST. Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochem. 2013; 48(7):1099-106.
  4. Djokovic V, Krsmanovic R, Bozanic DK, McPherson M, Van Tendeloo G, Nair PS, et al. Adsorption of sulfur onto a surface of silver nanoparticles stabilized with sago starch biopolymer. Colloids Surf B Biointerfaces. 2009; 73(1):30-5.
  5. Sanalibaba P, Cakmak GA. Exopolysaccharides production by lactic acid bacteria. Appl Microbiol Open Access. 2016; 2
  6. Surayot U, Wang J, Seesuriyachan P, Kuntiya A, Tabarsa M, Lee Y, et al. Exopolysaccharides from lactic acid bacteria: structural analysis, molecular weight effect on immunomodulation. Int J Biol Macromol. 2014; 68:233-40.
  7. Wang K, Niu M, Song D, Song X, Zhao J, Wu Y, et al. Preparation, partial characterization and biological activity of exopolysaccharides produced from Lactobacillus fermentum S1. J Biosci Bioeng. 2020; 129(2):206-14.
  8. Panghal A, Janghu S, Virkar K, Gat Y, Kumar V, Chhikara N. Potential non-dairy probiotic products – A healthy approach. Food Biosci. 2018; 21:80-9.
  9. Ciszek-Lenda M. Biological functions of exopolysaccharides from probiotic bacteria. Cent Eur J Immunol. 2011; 36:51-5.
  10. London LE, Kumar AH, Wall R, Casey PG, O'Sullivan O, Shanahan F, et al. Exopolysaccharide-producing probiotic Lactobacilli reduce serum cholesterol and modify enteric microbiota in ApoE-deficient mice. J Nutr. 2014; 144(12):1956-62.
  11. Torino MI, Font de Valdez G, Mozzi F. Biopolymers from lactic acid bacteria. Novel applications in foods and beverages. Front Microbiol. 2015; 6:834.
  12. Lynch KM, Coffey A, Arendt EK. Exopolysaccharide producing lactic acid bacteria: Their techno-functional role and potential application in gluten-free bread products. Food Res Int. 2018; 110:52-61.
  13. Daba GM, Elnahas MO, Elkhateeb WA. Contributions of exopolysaccharides from lactic acid bacteria as biotechnological tools in food, pharmaceutical, and medical applications. Int J Biol Macromol. 2021; 173:79-89.
  14. Bajpai VK, Majumder R, Rather I, Kim K. Extraction, isolation and purification of exopolysaccharide from lactic acid bacteria using ethanol precipitation method. Bangladesh J Pharmacol. 2016; 11:573.
  15. Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008; 3(2):163-75.
  16. Tetz GV, Artemenko NK, Tetz VV. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob Agents Chemother. 2009; 53(3):1204-9.
  17. Hanan MM, Saida MA. Purification And Characterization Of Exopolysaccharides (Eps) Extracted From Saccharomyces Cerevisiae. Egypt J Exp Biol. 2013; 9(2): 249-58.
  18. Dilna SV, Surya H, Aswathy RG, Varsha KK, Sakthikumar DN, Pandey A, et al. Characterization of an exopolysaccharide with potential health-benefit properties from a probiotic Lactobacillus plantarum RJF4. LWT-Food Sci Technol. 2015; 64(2):1179-86.
  19. Welman AD, Maddox IS. Fermentation performance of an exopolysaccharide-producing strain of Lactobacillus delbrueckii subsp. bulgaricus. J Ind Microbiol Biotechnol. 2003; 30(11):661-8.
  20. Abdalla AK, Ayyash MM, Olaimat AN, Osaili TM, Al-Nabulsi AA, Shah NP, et al. Exopolysaccharides as Antimicrobial Agents: Mechanism and Spectrum of Activity. Front Microbiol. 2021; 12:664395.
  21. Nguyen PT, Nguyen TT, Bui DC, Hong PT, Hoang QK, Nguyen HT. Exopolysaccharide production by lactic acid bacteria: the manipulation of environmental stresses for industrial applications. AIMS Microbiol. 2020; 6(4):451-69.
  22. Zhang J, Cao Y, Wang J, Guo X, Zheng Y, Zhao W, et al. Physicochemical characteristics and bioactivities of the exopolysaccharide and its sulphated polymer from Streptococcus thermophilus GST-6. Carbohydr Polym. 2016; 146:368-75.
  23. Riaz Rajoka MS, Wu Y, Mehwish HM, Bansal M, Zhao L. Lactobacillus exopolysaccharides: New perspectives on engineering strategies, physiochemical functions, and immunomodulatory effects on host health. Trends Food Sci Technol. 2020; 103:36-48.
  24. Wu MH, Pan TM, Wu YJ, Chang SJ, Chang MS, Hu CY. Exopolysaccharide activities from probiotic bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol. 2010; 144(1):104-10.
  25. Rani RP, Anandharaj M, David Ravindran A. Characterization of a novel exopolysaccharide produced by Lactobacillus gasseri FR4 and demonstration of its in vitro biological properties. Int J Biol Macromol. 2018; 109:772-83.
  26. Ayyash M, Abu-Jdayil B, Itsaranuwat P, Galiwango E, Tamiello-Rosa C, Abdullah H, et al. Characterization, bioactivities, and rheological properties of exopolysaccharide produced by novel probiotic Lactobacillus plantarum C70 isolated from camel milk. Int J Biol Macromol. 2020; 144:938-46.
  27. Sivasankar P, Seedevi P, Poongodi S, Sivakumar M, Murugan T, Sivakumar L, et al. Characterization, antimicrobial and antioxidant property of exopolysaccharide mediated silver nanoparticles synthesized by Streptomyces violaceus MM72. Carbohydr Polym. 2018; 181:752-9.
  28. Medrano M, Hamet MF, Abraham AG, Perez PF. Kefiran protects Caco-2 cells from cytopathic effects induced by Bacillus cereus infection. Antonie Van Leeuwenhoek. 2009; 96(4):505-13.
  29. Salachna P, Mizielinska M, Sobol M. Exopolysaccharide Gellan Gum and Derived Oligo-Gellan Enhance Growth and Antimicrobial Activity in Eucomis Plants. Polymers (Basel). 2018; 10(3)
  30. Zhou Y, Cui Y, Qu X. Exopolysaccharides of lactic acid bacteria: Structure, bioactivity and associations: A review. Carbohydr Polym. 2019; 207:317-32.
  31. Juraskova D, Ribeiro SC, Silva CCG. Exopolysaccharides Produced by Lactic Acid Bacteria: From Biosynthesis to Health-Promoting Properties. Foods. 2022; 11(2)
  32. Liu Z, Zhang Z, Qiu L, Zhang F, Xu X, Wei H, et al. Characterization and bioactivities of the exopolysaccharide from a probiotic strain of Lactobacillus plantarum WLPL04. J Dairy Sci. 2017; 100(9):6895-905.
  33. Xu X, Peng Q, Zhang Y, Tian D, Zhang P, Huang Y, et al. Antibacterial potential of a novel Lactobacillus casei strain isolated from Chinese northeast sauerkraut and the antibiofilm activity of its exopolysaccharides. Food Funct. 2020; 11(5):4697-706.
  34. Pan D, Mei X. Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohydr Polym. 2010; 80(3):908-14.
  35. Mahdhi A, Leban N, Chakroun I, Chaouch MA, Hafsa J, Fdhila K, et al. Extracellular polysaccharide derived from potential probiotic strain with antioxidant and antibacterial activities as a prebiotic agent to control pathogenic bacterial biofilm formation. Microb Pathog. 2017; 109:214-20.
  36. Kim Y, Oh S, Kim SH. Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun. 2009; 379(2):324-9.
  37. James KM, MacDonald KW, Chanyi RM, Cadieux PA, Burton JP. Inhibition of Candida albicans biofilm formation and modulation of gene expression by probiotic cells and supernatant. J Med Microbiol. 2016; 65(4):328-36.
  38. Jiang G, Gan L, Li X, He J, Zhang S, Chen J, et al. Characterization of Structural and Physicochemical Properties of an Exopolysaccharide Produced by Enterococcus sp. F2 From Fermented Soya Beans. Front Microbiol. 2021; 12:744007.
Archives of Razi Institute
Volume 77, Issue 6 - Serial Number 6
November and December 2022
Pages 2215-2221

Files

Share

How to cite

Statistics