Evaluation of Probiotic Properties of Pediococcus acidilactici M76 Producing Functional Exopolysaccharides and Its Lactic Acid Fermentation of Black Raspberry Extract
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strain and Growth Conditions
2.2. Acid and Bile Tolerance
2.3. Antimicrobial Activity
2.4. Cell Surface Hydrophobicity and Autoaggregation
2.5. Caenorhabditis elegans Intestinal Adhesion
2.6. In Vitro Immuno-Stimulatory Effects
2.6.1. Cell Culture and Bacterial Stimulation
2.6.2. Cell Viability Assay
2.6.3. qRT-PCR Analysis
2.7. Fermentation of BRE with PA-M76
2.8. Analysis of Cell Biomass and EPS
2.9. Total Anthocyanin, Phenol, and Flavonoid Analysis
2.10. In Vitro Antioxidant Activity
2.10.1. DPPH Radical Scavenging Activity
2.10.2. Lipid Peroxidation Inhibitory Activity
2.10.3. Radical Cation ABTS+ Scavenging Activity
2.11. Headspace Solid-Phase Microextraction (SPME) and Gas Chromatography-Mass Spectrometry (GC-MS) Analysis
2.12. Statistical Analysis
3. Results and Discussion
3.1. Fundamental Probiotic Properties: Tolerance and Antimicrobial Activity
3.2. Adhesion Properties of PA-M76
3.3. Immuno-Stimulatory Activity of PA-M76 to RAW 264.7 Cells
3.4. Black Raspberry Fermentation by PA-M76 Enhanced Production of Functional EPS
3.5. Phenolic Compounds and Antioxidant Activity of fBRE
3.6. Production of Volatile Compounds during Fermentation of BRE with P. acidilactici M76
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviation
BR | Black raspberry |
BRE | Black raspberry extract |
fBRE | Fermented black raspberry extract |
NfBRE | Non-fermented black raspberry extract |
EPS | Exopolysaccharide |
GIT | Gut intestinal track |
PA-M76 | Pediococcus acidilactici M76 |
PP | P. pentosaceus ATCC 33316 |
LGG | Lactobacillus rhamnosus GG |
PCA | Principal component analysis |
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Tolerance | PA-M76 | LGG | P. pentosaceus 33316 |
---|---|---|---|
pH 7.0 | 111.7 ± 0.58 | 110.7 ± 0.76 | 111.4 ± 0.35 |
pH 2.5 | 71.7 ± 0.22 | 72.5 ± 0.42 | 74.0 ± 0.08 |
Bile salt 0.3% | 101.8 ± 0.92 | 97.9 ± 0.78 | 95.9 ± 0.61 |
Bile salt 1% | 104.0 ± 1.11 | 93.3 ± 0.53 | 94.1 ± 0.78 |
Bile salt 3% | 101.4 ± 0.15 | 80.9 ± 1.73 | 89.1 ± 1.33 |
Temperature | 35~50 | 35~50 | 35~50 |
NaCl (%, w/v) | 4~8 | 4~7 | 4~8 |
Glucose (%, w/v) | 4~14 | 4~14 | 4~14 |
Strain | Pathogenic Microorganisms | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
S. aureus | S. epidermidis | S. xylosus | P. aeruginosa | P. putida | B. cereus | B. subtilis | B. vallismortis | E. coli | P. acnes | |
L. Rhamnosus GG * | ++++ | + | +++ | ++ | ++ | ++ | + | +++ | + | ++ |
P. acidilactici M76 | ++++ | +++ | +++ | +++ | +++ | ++++ | ++ | +++ | ++++ | +++ |
P. pentosaceus ATCC 33316 | ++++ | + | +++ | ++ | +++ | ++ | ++ | +++ | +++ | ++ |
Phenolic compounds | NfBRE | fBRE |
---|---|---|
Total polyphenols (mg GAE/100g) | 349.4 ± 3.99 a | 379.3 ± 4.38 b |
Total flavonoids (mg CE/100g) | 99.9 ± 2.37 a | 81 ± 0.82 a |
Total anthocyanins (TAC mg/L) | 43 ± 0.67 a | 45 ± 0.14 a |
Aroma Compound | RT (1) | Non Fermented Black Raspberry Extract (Day) | Fermented Black Raspberry Extract (Day) | Odor Description (2) | ||||||
---|---|---|---|---|---|---|---|---|---|---|
0 | 1 | 2 | 3 | 0 | 1 | 2 | 3 | |||
Acids | ||||||||||
Acetic acid | 2.77 | nd (3) | nd | nd | nd | nd | nd | 0.03 ± 0.01 ab | 0.05 ± 0.03 a | Sour |
Octanoic acid | 6.63 | nd | nd | nd | nd | nd | nd | 0.18 ± 0.16 a | 0.08 ± 0.07 ab | Fatty, waxy, cheesy |
Decanoic acid | 8.01 | nd | 0.01 ± 0.01 | 0.01 ± 0.00 | nd | nd | 0.32 ± 0.28 | 0.07 ± 0.06 | 0.02 ± 0.01 | Rancid, sour, fatty, citrus |
Alcohols | ||||||||||
Isoamyl alcohol | 2.93 | nd | nd | nd | nd | nd | 0.65 ± 0.19 b | 1.48 ± 0.25 a | 1.75 ± 0.34 a | Alcoholic, whiskey, fruity |
2,3-Butanediol | 3.62 | nd | nd | nd | nd | nd | nd | 0.01 ± 0.01 ab | 0.02 ± 0.01 a | Fruity, creamy, buttery |
2-Ethyl-1-hexanol | 5.48 | nd | nd | nd | nd | nd | nd | nd | 0.05 ± 0.00 | Citrus, floral, oily, sweet |
Phenylethyl alcohol | 6.25 | 0.02 ± 0.00 b | 0.02 ± 0.01 Ba | 0.02 ± 0.01 Ba | 0.02 ± 0.01 Ba | 0.05 ± 0.02 Ab | 0.40 ± 0.25 Aab | 0.48 ± 0.21 Aa | 0.64 ± 0.31 Aa | Floral, rose, dried rose |
Cherry propanol | 6.79 | 0.15 ± 0.01 | 0.17 ± 0.03 | 0.16 ± 0.04 | 0.15 ± 0.02 | 0.12 ± 0.02 | nd | nd | nd | Sweet, fruity, cherry |
Aldehyde | ||||||||||
Benzealdehyde | 4.95 | 0.01 ± 0.01 Ab | 0.03 ± 0.00 Aa | 0.04 ± 0.00 a | 0.04 ± 0.00 a | nd | nd | nd | nd | Sharp, sweet, bitter, almond |
Esters | ||||||||||
Ethyl acetate | 2.11 | nd | nd | nd | nd | nd | 1.99 ± 0.30 | 1.60 ± 0.85 | 2.08 ± 0.54 | Ethereal, fruity, sweet, grape |
Isoamyl acetate | 4.14 | nd | nd | nd | nd | nd | 0.30 ± 0.07 b | 0.63 ± 0.11 a | 0.49 ± 0.11 a | Sweet, banana, fruity |
Ethyl hexanoate | 5.22 | nd | nd | nd | nd | nd | 0.15 ± 0.12 | 0.13 ± 0.10 | 0.14 ± 0.12 | Sweet, fruity, pineapple |
Ethyl benzoate | 6.67 | nd | nd | nd | nd | nd | nd | nd | 0.05 ± 0.01 | Fruity, sweet, wintergreen, minty |
Ethyl octanoate | 6.82 | nd | nd | nd | nd | nd | 1.11 ± 0.94 | 0.89 ± 0.73 | 0.75 ± 0.60 | Fruity, winey, waxy, sweet |
Phenethyl acetate | 7.31 | nd | nd | nd | nd | nd | nd | 0.17 ± 0.15 | 0.18 ± 0.16 | Floral, rose, sweet, honey |
Ethyl nonanoate | 7.53 | nd | nd | nd | nd | nd | 0.02 ± 0.02 | 0.04 ± 0.04 | 0.07 ± 0.05 | Fruity, rose, waxy, rummy |
Ethyl 9-decenoate | 8.16 | nd | nd | nd | nd | nd | 0.50 ± 0.44 | 0.23 ± 0.20 | 0.13 ± 0.11 | Fruity, fatty |
Ethyl decanoate | 8.21 | nd | 0.04 ± 0.05 | 0.03 ± 0.04 | 0.01 ± 0.02 | nd | 0.52 ± 0.44 | 0.45 ± 0.38 | 0.36 ± 0.30 | Sweet, waxy, fruity, apple |
Isoamyl octanoate | 8.55 | nd | nd | nd | nd | nd | 0.05 ± 0.04 | 0.04 ± 0.04 | 0.03 ± 0.02 | Sweet, oily, fruity, green |
Ethyl dodecanoate | 9.46 | nd | nd | nd | nd | nd | 0.05 ± 0.05 | 0.08 ± 0.06 | 0.10 ± 0.08 | Sweet, waxy, floral, soapy |
Ethyl palmitate | 11.6 | nd | nd | nd | nd | nd | nd | nd | 0.01 ± 0.00 | Waxy, fruity, creamy, milky |
Terpenes | ||||||||||
p-Cymene | 5.5 | 0.07 ± 0.01 a | 0.03 ± 0.00 Ab | 0.02 ± 0.02 b | nd | 0.05 ± 0.01 a | 0.02 ± 0.00 Bb | nd | nd | Fresh, citrus, terpenic |
Linalool | 6.08 | 0.09 ± 0.01 a | 0.06 ± 0.01 Ab | 0.05 ± 0.01 Abc | 0.03 ± 0.00 Ac | 0.07 ± 0.02 a | 0.04 ± 0.01 Bb | 0.02 ± 0.01 Bb | 0.02 ± 0.00 Bb | Citrus, floral, sweet |
Terpinen-4-ol | 6.76 | nd | 0.18 ± 0.01 a | 0.16 ± 0.02 b | 0.12 ± 0.01 c | nd | nd | nd | nd | Peppery, woody, earthy |
alpha-terpineol | 6.85 | 0.35 ± 0.02 a | 0.34 ± 0.02 Aab | 0.31 ± 0.03 Abc | 0.27 ± 0.02 Ac | 0.29 ± 0.03 a | 0.14 ± 0.13 Bb | 0.13 ± 0.04 Bb | 0.15 ± 0.02 Bb | Pine, terpenic, lilac, citrus |
Myrtenol | 6.91 | 0.18 ± 0.01 a | 0.16 ± 0.01 ab | 0.13 ± 0.01 b | 0.11 ± 0.01 c | 0.18 ± 0.02 a | 0.13 ± 0.06 ab | 0.10 ± 0.03 b | 0.08 ± 0.02 b | Woody, pine, balsamic |
Nerol | 7.25 | 0.02 ± 0.00 a | 0.01 ± 0.00 b | 0.01 ± 0.00 c | 0.01 ± 0.00 a | 0.02 ± 0.00 a | nd | 0.01 ± 0.00 b | 0.01 ± 0.00 b | Fresh, citrus, floral |
Farnesol | 10.24 | nd | nd | nd | nd | nd | nd | nd | 0.01 ± 0.01 | Sweet, floral |
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Song, Y.-R.; Lee, C.-M.; Lee, S.-H.; Baik, S.-H. Evaluation of Probiotic Properties of Pediococcus acidilactici M76 Producing Functional Exopolysaccharides and Its Lactic Acid Fermentation of Black Raspberry Extract. Microorganisms 2021, 9, 1364. https://doi.org/10.3390/microorganisms9071364
Song Y-R, Lee C-M, Lee S-H, Baik S-H. Evaluation of Probiotic Properties of Pediococcus acidilactici M76 Producing Functional Exopolysaccharides and Its Lactic Acid Fermentation of Black Raspberry Extract. Microorganisms. 2021; 9(7):1364. https://doi.org/10.3390/microorganisms9071364
Chicago/Turabian StyleSong, Young-Ran, Chan-Mi Lee, Seon-Hye Lee, and Sang-Ho Baik. 2021. "Evaluation of Probiotic Properties of Pediococcus acidilactici M76 Producing Functional Exopolysaccharides and Its Lactic Acid Fermentation of Black Raspberry Extract" Microorganisms 9, no. 7: 1364. https://doi.org/10.3390/microorganisms9071364
APA StyleSong, Y. -R., Lee, C. -M., Lee, S. -H., & Baik, S. -H. (2021). Evaluation of Probiotic Properties of Pediococcus acidilactici M76 Producing Functional Exopolysaccharides and Its Lactic Acid Fermentation of Black Raspberry Extract. Microorganisms, 9(7), 1364. https://doi.org/10.3390/microorganisms9071364