Comparative Chemical Analysis and Bioactive Properties of Aqueous and Glucan-Rich Extracts of Three Widely Appreciated Mushrooms: Agaricus bisporus (J.E.Lange) Imbach, Laetiporus sulphureus (Bull.) Murill and Agrocybe aegerita (V. Brig.) Vizzini
Abstract
:1. Introduction
2. Results and Discussion
2.1. Total α-Glucan and β-Glucan Content in AE and PE
2.2. Total Protein Content of AE and PE
2.3. Total Phenolic Content (TPC) of AE and PE
2.4. Protein Profile of Mushroom AE
2.5. UHPLC–QToF-MS Profiling of Mushroom Extracts
2.6. ATR-FTIR Spectroscopy of Mushroom AE and PE
2.7. Antioxidant Activity
2.8. Cytotoxicity of Extracts
2.9. Wound-Healing Properties of Extracts
2.10. Anti-Inflammatory Properties of Extracts
2.11. Antimicrobial Activity Assays
2.11.1. Antibacterial Activity
Microorganisms | A. aegerita AE | A. bisporus AE | L. sulphureus AE | A. aegerita PE | A. bisporus PE | L. sulphureus PE | E211 | E224 | |
---|---|---|---|---|---|---|---|---|---|
S. aureus (ATCC 11632) | MIC | 4.00 c | 4.00 c | 4.00 c | 4.00 c | 2.00 b | 4.00 c | 4.00 c | 1.00 a |
MBC | 8.00 c | 8.00 c | 8.00 c | 8.00 c | 4.00 b | 8.00 c | 4.00 b | 1.00 a | |
B. cereus (clinical isolate) | MIC | 1.00 b | 2.00 c | 2.00 c | 4.00 d | 2.00 b | 4.00 c | 0.50 a | 2.00 b |
MBC | 2.00 b | 4.00 c | 4.00 c | 8.00 d | 4.00 c | 8.00 d | 0.50 a | 4.00 c | |
L. monocytogenes (NCTC 7973) | MIC | 4.00 d | 4.00 d | 2.00 c | 4.00 d | 2.00 c | 4.00 d | 1.00 b | 0.50 a |
MBC | 8.00 d | 8.00 d | 4.00 c | 8.00 d | 4.00 c | 8.00 d | 2.00 b | 1.00 a | |
L. monocytogenes (ATCC 13932) | MIC | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 0.50 a | 0.50 a |
MBC | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 1.00 a | 1.00 a | |
L. monocytogenes (ATCC 15313) | MIC | 0.50 a | 0.50 a | 0.50 a | 0.50 a | 1.00 b | 0.50 a | 0.50 a | 1.00 b |
MBC | 1.00 a | 1.00 a | 1.00 a | 1.00 a | 2.00 b | 1.00 a | 1.00 a | 2.00 b | |
L. monocytogenes (ATCC 19111) | MIC | 1.00 a | 1.00 a | 1.00 a | 1.00 a | 1.00 a | 1.00 a | 1.00 a | 1.00 a |
MBC | 2.00 a | 2.00 a | 2.00 a | 2.00 a | 2.00 a | 2.00 a | 2.00 a | 2.00 a | |
L. monocytogenes (ATCC 35152) | MIC | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 0.50 a | 1.00 b |
MBC | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 1.00 a | 2.00 b | |
Y. enterocolitica (ATCC 23715) | MIC | 0.50 b | 0.25 a | 0.50 b | 0.50 b | 0.50 b | 0.50 b | 0.50 b | 0.50 b |
MBC | 1.00 b | 0.50 a | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | |
Y. enterocolitica (ATCC 9610) | MIC | 0.50 b | 0.50 b | 0.25 a | 0.50 b | 0.25 a | 0.25 a | 1.00 c | 0.50 b |
MBC | 1.00 b | 1.00 b | 0.50 a | 1.00 b | 0.50 a | 1.00 b | 2.00 c | 1.00 b | |
E. coli (ATCC 25922) | MIC | 4.00 d | 4.00 d | 2.00 c | 4.00 d | 2.00 c | 4.00 d | 1.00 b | 0.50 a |
MBC | 8.00 d | 8.00 d | 4.00 c | 8.00 d | 4.00 c | 8.00 d | 2.00 b | 1.00 a | |
E. coli (ATCC 11775) | MIC | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 0.50 a | 0.50 a |
MBC | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 1.00 a | 1.00 a | |
E. coli O157:H (ATCC 700728) | MIC | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 0.50 a |
MBC | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 1.00 a | |
E. coli O157:H (ATCC 43888) | MIC | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 1.00 b | 0.50 a | 1.00 b |
MBC | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 2.00 b | 1.00 a | 2.00 b | |
S. Typhimurium (ATCC 13311) | MIC | 4.00 c | 4.00 c | 2.00 b | 4.00 c | 2.00 b | 4.00 c | 1.00 a | 1.00 a |
MBC | 8.00 d | 8.00 d | 4.00 c | 8.00 d | 4.00 c | 8.00 d | 2.00 b | 1.00 a | |
E. cloacae (ATCC 35030) | MIC | 4.00 c | 8.00 d | 2.00 b | 4.00 c | 2.00 b | 4.00 c | 2.00 b | 0.50 a |
MBC | 8.00 c | 8.00 c | 4.00 b | 8.00 c | 4.00 b | 8.00 c | 4.00 b | 0.50 a |
2.11.2. Antifungal Activity of Extracts
A. fumigatus (ATCC 9197) | A. versicolor (ATCC 11730) | A. niger (ATCC 6275) | P. funiculosum (ATCC 36839) | P. verrucosum var. cyclopium (food isolate) | T. viride (IAM 5061) | ||
---|---|---|---|---|---|---|---|
A. aegerita AE | MIC | 2.00 c | 2.00 c | 1.00 a | 2.00 c | 2.00 b | 1.00 b |
MFC | 4.00 | 4.00 c | 2.00 b | 4.00 c | 4.00 b | 2.00 b | |
A. bisporus AE | MIC | 1.00 b | 2.00 c | 1.00 a | 2.00 c | 2.00 b | 1.00 b |
MFC | 2.00 b | 4.00 c | 2.00 b | 4.00 c | 4.00 b | 2.00 b | |
L. sulphureus AE | MIC | 0.50 a | 1.00 b | 1.00 a | >8.00 e | >8.00 c | 1.00 b |
MFC | 1.00 a | 2.00 b | 2.00 b | >8.00 e | >8.00 c | 2.00 b | |
A. aegerita PE | MIC | 0.50 a | 0.50 a | 1.00 a | 4.00 d | >8.00 c | 1.00 b |
MFC | 1.00 a | 1.00 a | 2.00 b | 8.00 d | >8.00 c | 2.00 b | |
A. bisporus PE | MIC | >8.00 c | 2.0 0c | >8.00 b | 4.00 d | >8.00 c | 1.00 b |
MFC | >8.00 c | 2.00 b | >8.00 c | 8.00 d | >8.00 c | 2.00 b | |
L. sulphureus PE | MIC | 0.50 a | 0.50 a | 1.00 a | 4.00 d | >8.00 c | 1.00 b |
MFC | 1.00 a | 1.00 a | 2.00 b | 8.00 d | >8.00 c | 2.00 b | |
E211 | MIC | 1.00 b | 2.00 c | 1.00 a | 1.00 b | 2.00 b | 1.00 b |
MFC | 2.00 b | 4.00 c | 2.00 b | 2.00 b | 4.00 b | 2.00 b | |
E224 | MIC | 1.00 b | 1.00 b | 1.00 a | 0.50 a | 1.00 a | 0.50 a |
MFC | 1.00 a | 1.00 a | 1.00 a | 0.50 a | 1.00 a | 0.50 a |
2.11.3. Antibiofilm Activity
3. Material and Methods
3.1. Standards and Reagents
3.2. Mushroom Collection and Identification
3.3. Preparation of Mushroom Extracts
3.4. Total α-Glucan and β-Glucan Content
3.5. Total Protein Content
3.6. Total Phenolic Content
3.7. Protein Profile of Mushroom Aqueous Extracts
3.8. Phenolic Profile of Mushroom Aqueous Extracts
3.8.1. Preparation of Samples
3.8.2. UHPLC–QToF-MS Analysis
3.9. ATR-FTIR Spectroscopy
3.10. Antioxidant Assay
3.10.1. FRAP Assay
3.10.2. ABTS•+ Assay
3.10.3. DPPH• Assay
3.11. Cytotoxicity towards HaCaT Cells
3.12. Scratch Wound-Healing Assay
3.13. Anti-Inflammatory Properties
3.14. Antimicrobial Activity Assay
3.14.1. Microorganisms
3.14.2. Antibacterial Activity and Anticandidal Activity
3.14.3. Antifungal Activity
3.14.4. Inhibition of Biofilm Formation
3.15. Statistical Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Total Glucan Content (%) | α-Glucans (%) | β-Glucans (%) | |
---|---|---|---|
Polysaccharide extracts | |||
A. aegerita | 44.28 ± 0.06 | 9.34 ± 0.86 | 34.95 ± 0.80 |
A. bisporus | 33.37 ± 0.31 | 12.64 ± 1.82 | 20.73 ± 2.13 |
L. sulphureus | 11.47 ± 0.38 | 0.74 ± 0.03 | 10.73 ± 0.35 |
Aqueous extracts | |||
A. aegerita | 25.47 ± 2.22 | 14.36 ± 0.57 | 11.10 ± 2.79 |
A. bisporus | 7.32 ± 0.07 | 2.54 ± 0.02 | 4.77 ± 0.09 |
L. sulphureus | 6.92 ± 1.45 | 2.27 ± 0.03 | 4.65 ± 0.05 |
Total Protein Content (g BSA/100 g dw) | ||
---|---|---|
Aqueous Extracts | Polysaccharide Extracts | |
A. aegerita | 1.84 ± 0.02 | n.d. * |
A. bisporus | 2.70 ± 0.07 | n.d. * |
L. sulphureus | 5.62 ± 0.91 | n.d. * |
Total Phenolic Content (g GAE/100 g dw) | ||
---|---|---|
Aqueous Extracts | Polysaccharide Extracts | |
A. aegerita | 23.72 ± 0.02 | n.d. * |
A. bisporus | 7.9 ± 0.07 | n.d. * |
L. sulphureus | 0.93 ± 0.91 | 0.19 ± 0.01 |
RT, min | Compounds Name | Formula | Calculated Mass | m/z Exact Mass | mDa | MS2 Fragments (% Base Peak) | Samples | Refs | |||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
ABP | ABA | AAP | AAA | LSP | LSA | ||||||||
Organic acids and derivatives | |||||||||||||
0.73 | Fumaric acid | C4H3O4– | 115.00368 | 115.00491 | −1.23 | / | + | + | + | + | − | + | [22,23] |
0.73 | Malic acid | C4H5O5– | 133.01425 | 133.01571 | −1.46 | 115.0050 (100) | + | + | + | + | + | + | [22,23] |
0.83 | Citric acid | C6H7O7– | 191.01973 | 191.02299 | −3.26 | 111.0093 (100), 112.01131 | + | + | + | + | + | + | [22,23] |
0.94 | Succinic acid | C4H5O4– | 117.01933 | 117.02020 | −0.87 | / | + | + | − | + | + | + | [22] |
6.27 | Pimelic acid (6-Carboxyhexanoate) | C7H11O4– | 159.06628 | 159.06686 | −0.58 | 115.07504 (100), 116.08119, 118.04377 | − | + | − | + | + | + | / |
7.88 | 3-hydroxy sebacic acid | C10H17O5– | 217.10815 | 217.10986 | −1.72 | 171.1020 (100), 127.1115, 132.04799, 153.06758 | − | + | − | − | + | + | [33] |
8.49 | Azelaic acid | C9H15O4– | 187.09758 | 187.09846 | −0.88 | 123.0813 (100), 125.0971 | + | + | + | + | + | + | [24] |
8.56 | Diethyl 3-hydroxyglutarate | C9H15O5– | 203.09250 | 203.09342 | −0.92 | 113.0977 (100), 129.0912, 141.0931, 147.0154 | − | − | − | + | + | + | / |
9.31 | Sebacic acid | C10H17O4– | 201.11323 | 201.11399 | −0.76 | 139.1132 (100), 111.0815, 137.0974, 183.1025, 184.1039 | − | + | + | + | + | + | [24] |
10.58 | Pinellic acid | C18H33O5– | 329.23335 | 329.23534 | −2.00 | 171.1047 (100), 139.1139, 183.1382, 201.1145, 211.1345, 229.1449 | + | + | + | + | + | + | [25] |
13.41 | 9-Hydroxy-13-oxo-10-octadecenoic acid | C18H31O4– | 311.22278 | 311.22509 | −2.31 | 201.1138 (100), 127.1115, 139.1125, 171.1032, 183.1325, 197.1195 | − | + | − | + | + | + | [26] |
15.84 | 13-Hydroxy-9,11-octadecadienoic acid | C18H31O3– | 295.22787 | 295.22894 | −1.07 | 127.1132 (100), 111.0818, 171.1024, 183.1032 | + | + | + | + | + | + | [26] |
Phenolic acids and derivatives | |||||||||||||
1.28 | Gallic acid | C7H5O5– | 169.01425 | 169.01871 | −4.46 | 125.0240 (100), 124.0164, 107.0145, 108.0226 | − | − | − | − | + | − | [27] |
2.49 | 3,4-Dihydroxybenzoic acid (like Protocatehuic acid) | C7H5O4– | 153.01933 | 153.02228 | −2.95 | 108.0215 (100), 109.0295 | − | + | − | − | + | + | [27,28] |
4.30 | p-Hydroxybenzoic acid | C7H5O3– | 137.02390 | 137.02649 | −2.59 | / | − | + | − | + | + | + | [27,28] |
4.31 | 4-Methoxybenzoic acid (like p-Anisic acid) | C8H7O3– | 151.04007 | 151.04025 | −0.18 | 108.0219 (100), 107.0389, 109.0327 | − | − | − | + | − | + | [29] |
4.44 | 3,4-Dimethoxybenzoate (like veratric acid) | C9H9O4– | 181.05063 | 181.05262 | −1.98 | 134.0381 (100), 107.0569, 135.0427, 137.0216, 119.0531 | − | − | − | + | + | + | [30] |
6.19 | Coumaric acid is. I | C9H7O3– | 163.04007 | 163.04142 | −1.35 | 117.0338 (100), 118.0352, 119.0237 | − | − | − | + | − | + | [27,28] |
7.28 | p-hydroxy-hydrocinnamic acid (or Dihydrocoumaric acid) | C9H9O3– | 165.05572 | 165.05574 | −0.02 | 119.0504 (100), 117.0343, 147.0475 | − | + | − | + | + | + | / |
7.58 | Vanillic acid | C8H7O4– | 167.03498 | 167.03916 | −4.18 | 105.0345 (100), 123.0457 | − | − | − | − | + | + | [30,31] |
7.81 | Sinapic acid | C11H11O5– | 223.06120 | 223.06138 | −0.18 | 164.0408 (100), 117.0675, 133.0661, 163.0411, 179.0703, 193.0171 | − | + | − | + | − | − | [31] |
9.77 | Coumaric acid is. II | C9H7O3– | 163.04007 | 163.04023 | −0.17 | 117.0357 (100), 119.0454, 145.9088 | − | − | − | + | − | + | [28,30] |
11.80 | Ethyl-homovanillate | C11H13O4– | 209.08193 | 209.08451 | −2.58 | 122.0374 (100), 135.0455, 150.0693 | − | − | − | − | + | − | / |
Other compounds | |||||||||||||
13.82 | Triterpenoid (like maslinic acid) | C30H47O4– | 471.34798 | 471.34992 | −1.94 | 471.3453 (100) | − | − | − | − | + | + | [32] |
Mushroom Extracts | ABTS (g Trolox/100 g) | FRP (µg AA/mL) | FCC (µg EDTA/mL) |
---|---|---|---|
A. aegerita, aqueous | 21.97 | 43.56 | 48.25 |
A. bisporus, aqueous | 9.07 | 7.26 | 47.9 |
L. sulphureus, aqueous | 4.92 | 219.52 | 0.19 |
L. sulphureus, polysaccharides | 3.37 | 42.05 | 2.49 |
Mushroom Extracts | IC50 Value (µg/mL) |
---|---|
A. bisporus, aqueous | 246.24 ± 5.46 |
L. sulphureus, aqueous | 274.72 ± 2.54 |
A. aegerita, aqueous | >400 |
A. bisporus, polysaccharides | >400 |
L. sulphureus, polysaccharides | >400 |
A. aegerita, polysaccharides | >400 |
Mushroom Extracts | Wound Closure % |
---|---|
A. bisporus, aqueous | 65.96 ± 6.98 |
L. sulphureus, aqueous | 62.56 ± 9.43 |
A. bisporus, polysaccharides | 84.27 ± 4.54 |
L. sulphureus, polysaccharides | 77.06 ± 7.65 |
Mushroom Extracts | IL-6 (pg/mL) |
---|---|
Control | 2.96 ± 0.02 |
S. aureus | 16.64 ± 0.06 |
S. aureus + AE A. aegerita | 4.56 ± 0.08 |
S. aureus + PE A. aegerita | 4.21 ± 0.02 |
S. aureus + AE A. bisporus | 7.42 ± 0.02 |
S. aureus + PE A. bisporus | 6.78 ± 0.04 |
S. aureus + AE L. sulphureus | 15.12 ± 0.10 |
S. aureus + PE L. sulphureus | 10.21 ± 0.09 |
C. albicans 475/15 | C. albicans 13/15 | C. albicans 17/15 | C. parapsilosis ATCC 22019 | C. tropicalis ATCC 750 | C. krusei H1/16 | ||
---|---|---|---|---|---|---|---|
A. aegerita AE | MIC | 2.00 d | 2.00 d | 2.00 b | 1.00 b | 2.00 c | 4.00 c |
MFC | 4.00 d | 4.00 d | 4.00 b | 2.00 b | 4.00 c | 8.00 c | |
A. bisporus AE | MIC | 1.00 c | 2.00 d | 2.00 b | 1.00 b | 2.00 c | 4.00 c |
MFC | 2.00 c | 4.00 d | 4.00 b | 2.00 b | 4.00 c | 8.00 c | |
L. sulphureus AE | MIC | 0.50 b | 0.50 b | 4.00 c | 1.00 b | 1.00 b | 4.00 c |
MFC | 1.00 b | 1.00 b | 8.00 c | 2.00 b | 2.00 b | 8.00 c | |
A. aegerita PE | MIC | 0.50 b | 0.50 b | 2.00 b | 1.00 b | 2.00 c | 4.00 c |
MFC | 1.00 b | 1.00 b | 4.00 b | 2.00 b | 4.00 c | 8.00 c | |
A. bisporus PE | MIC | 1.00 c | 1.00 c | 2.00 b | 1.00 b | 2.00 c | 2.00 b |
MFC | 2.00 c | 2.00 c | 4.00 b | 2.00 b | 4.00 c | 4.00 b | |
L. sulphureus PE | MIC | 0.50 b | 1.00 c | 2.00 b | 1.00 b | 2.00 c | 2.00 b |
MFC | 1.00 b | 2.00 c | 4.00 b | 2.00 b | 4.00 c | 4.00 b | |
Ketoconazole (× 10−3) | MIC | 3.20 a | 1.60 a | 1.60 a | 3.20 a | 1.60 a | 1.60 a |
MFC | 6.40 a | 51.20 a | 51.20 a | 6.40 a | 6.40 a | 3.20 a |
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Petrović, J.; Glamočlija, J.; Milinčić, D.D.; Doroški, A.; Lević, S.; Stanojević, S.P.; Kostić, A.Ž.; Minić, D.A.P.; Vidović, B.B.; Plećić, A.; et al. Comparative Chemical Analysis and Bioactive Properties of Aqueous and Glucan-Rich Extracts of Three Widely Appreciated Mushrooms: Agaricus bisporus (J.E.Lange) Imbach, Laetiporus sulphureus (Bull.) Murill and Agrocybe aegerita (V. Brig.) Vizzini. Pharmaceuticals 2024, 17, 1153. https://doi.org/10.3390/ph17091153
Petrović J, Glamočlija J, Milinčić DD, Doroški A, Lević S, Stanojević SP, Kostić AŽ, Minić DAP, Vidović BB, Plećić A, et al. Comparative Chemical Analysis and Bioactive Properties of Aqueous and Glucan-Rich Extracts of Three Widely Appreciated Mushrooms: Agaricus bisporus (J.E.Lange) Imbach, Laetiporus sulphureus (Bull.) Murill and Agrocybe aegerita (V. Brig.) Vizzini. Pharmaceuticals. 2024; 17(9):1153. https://doi.org/10.3390/ph17091153
Chicago/Turabian StylePetrović, Jovana, Jasmina Glamočlija, Danijel D. Milinčić, Ana Doroški, Steva Lević, Slađana P. Stanojević, Aleksandar Ž. Kostić, Dušanka A. Popović Minić, Bojana B. Vidović, Ana Plećić, and et al. 2024. "Comparative Chemical Analysis and Bioactive Properties of Aqueous and Glucan-Rich Extracts of Three Widely Appreciated Mushrooms: Agaricus bisporus (J.E.Lange) Imbach, Laetiporus sulphureus (Bull.) Murill and Agrocybe aegerita (V. Brig.) Vizzini" Pharmaceuticals 17, no. 9: 1153. https://doi.org/10.3390/ph17091153