Bioconversion of Grape Pomace with Rhizopus oryzae under Solid-State Conditions: Changes in the Chemical Composition and Profile of Phenolic Compounds
Abstract
:1. Introduction
2. Materials and Methods
2.1. Standards and Reagents
2.2. Substrate and Microorganism
2.3. Biological Treatment of Grape Pomace by Rhizopus oryzae
2.4. pH Measurement
2.5. Chemical Composition of Grape Pomace
2.5.1. Reducing Sugars
2.5.2. Biomass Concentration
2.5.3. Analysis of Minerals and Undesirable Substances
2.6. Determination of Antioxidant Activity
2.7. Measurements of Enzyme Activities
2.7.1. Preparation of Crude Enzyme Extracts
2.7.2. Assays for Measuring Enzyme Activity
2.8. Statistical Analysis
3. Results and Discussion
3.1. Biological Treatment of Grape Pomace by R. oryzae in a Tray Bioreactor
3.2. Chemical Composition of Grape Pomace
3.2.1. Lignocellulosic Components
3.2.2. Sugars Content
3.2.3. Ash, Proteins, Total Organic Carbon, Total Nitrogen, and Free Fats Content
3.2.4. Loss of the Total Substrate Mass
3.2.5. Biomass Concentration
3.2.6. Minerals and Undesirable Substances in Grape Pomace
3.2.7. Content of Total Phenolic Compounds (TPC), Total Flavonoids (TF), Total Extractable Proanthocyanidins (TPA), and Antioxidant Activity of GP Extracts
3.2.8. The Effect of Biological Treatment by R. oryzae on the Recovery of Individual Phenolic Compounds from Grape Pomace
3.2.9. Correlation between Hydrolytic and Lignolytic Enzymes and Individual Phenolic Compounds from Grape Pomace
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Enzyme | Buffer | pH |
---|---|---|
Xylanase | 50 mM sodium citrate buffer | 5.3 |
Cellulase | 50 mM sodium citrate buffer | 4.8 |
β-glucosidase | 100 mM sodium acetate buffer | 5.0 |
Invertase | 100 mM sodium acetate buffer | 4.5 |
Laccase | 50 mM sodium malonate buffer | 4.5 |
Manganese peroxidase (MnP) | 50 mM sodium malonate buffer | 4.5 |
Lignin peroxidase (LiP) | 50 mM sodium tartrate buffer | 3.0 |
Compound | GP | SSF in Laboratory Jars | SSF in a Tray Bioreactor | ||||
---|---|---|---|---|---|---|---|
Day “0” | Day 5 | Day 10 | Day 15 | Day 5 | Day 10 | Day 15 | |
Ash (%db) | 8.65 ± 0.00 c | 8.19 ± 0.11 bc | 8.30 ± 0.18 bc | 7.59 ± 0.73 a | 7.84 ± 0.14 ab | 8.13 ± 0.09 abc | 7.95 ± 0.08 ab |
Proteins (%db) | 11.35 ± 0.09 e | 9.09 ± 0.18 b | 8.41 ± 0.10 a | 9.91 ± 0.10 d | 9.41 ± 0.00 c | 9.56 ± 0.10 c | 11.31 ± 0.10 e |
Free fats (%db) | 7.50 ± 0.20 a | 9.01 ± 0.29 b | 10.66 ± 0.29 d | 10.77 ± 0.10 d | 11.13 ± 0.47 d | 11.00 ± 0.03 d | 9.73 ± 0.04 c |
TOCGP (%db) | 72.18 ± 0.56 a | 73.03 ± 0.20 ab | 73.77 ± 1.17 bc | 74.75 ± 0.21 cd | 74.20 ± 0.56 c | 75.33 ± 0.12 d | 80.14 ± 0.47 e |
NDF (%db) | 52.81 ± 1.10 a | 57.60 ± 0.64 b | 58.64 ± 1.12 b | 56.69 ± 0.20 b | 53.16 ± 1.13 a | 58.78 ± 1.44 b | 61.72 ± 1.84 c |
ADF (%db) | 44.26 ± 2.41 a | 52.18 ± 0.77 bc | 52.84 ± 0.66 c | 50.17 ± 0.55 b | 44.84 ± 1.77 a | 49.66 ± 1.40 b | 50.60 ± 0.94 bc |
ADL/lignin (%db) | 31.35 ± 1.49 a | 36.59 ± 0.72 cd | 37.97 ± 0.33 d | 34.28 ± 0.57 c | 30.81 ± 0.26 a | 35.45 ± 0.14 bc | 37.11 ± 1.01 d |
Hemicellulose (%db) | 8.55 ± 1.68 c | 5.42 ± 0.30 a | 5.80 ± 1.72 a | 6.52 ± 0.76 ab | 8.32 ± 0.64 bc | 9.12 ± 1.11 c | 11.64 ± 0.20 d |
Cellulose (%db) | 12.90 ± 1.70 a | 15.58 ± 0.05 bc | 14.87 ± 0.27 bc | 15.89 ± 0.01 c | 14.03 ± 1.58 ab | 14.97 ± 0.57 bc | 13.96 ± 0.55 ab |
Sucrose (mg/gdb) | 12.04 ± 0.27 e | 6.21 ± 0.03 d | 4.77 ± 0.03 e | 4.28 ± 0.02 b | 2.88 ± 0.09 a | 4.40 ± 0.03 b | 4.88 ± 0.14 c |
Glucose (mg/gdb) | 7.01 ± 0.29 e | 1.63 ± 0.04 b | 2.13 ± 0.07 c | 0.78 ± 0.49 a | 1.98 ± 0.04 bc | 2.64 ± 0.11 d | 2.14 ± 0.16 c |
Fructose (mg/gdb) | 1.50 ± 0.12 d | 0.21 ± 0.02 bc | 0.07 ± 0.01 a | 0.15 ± 0.01 ab | 0.30 ± 0.01 c | 0.18 ± 0.01 b | 0.19 ± 0.07 b |
RS (mgGLUCOSE/gdb) | 30.00 ± 0.76 g | 21.93 ± 0.20 f | 18.77 ± 0.19 d | 13.96 ± 0.01 c | 19.78 ± 0.41 e | 13.08 ± 0.37 b | 9.19 ± 0.41 a |
TOCE (mg/gdb) | 79.25 ± 7.15 d | 49.65 ± 1.30 b | 45.27 ± 1.13 b | 30.54 ± 1.18 a | 63.78 ± 1.40 c | 44.90 ± 0.47 b | 26.50 ± 0.20 a |
TN (mg/gdb) | 1.45 ± 0.00 e | 0.85 ± 0.02 d | 0.72 ± 0.02 c | 0.41 ± 0.04 a | 0.90 ± 0.02 d | 0.66 ± 0.03 b | 0.36 ± 0.04 a |
Element | Unit | Content | |
---|---|---|---|
Day “0” | Day 15 | ||
Phosphorus (P) | % | 0.30 | 0.28 |
Calcium (Ca) | mg/kg | 4967 | 5030 |
Potassium (K) | mg/kg | 22,130 | 11,219 |
Iron (Fe) | mg/kg | 103 | 87 |
Lead (Pb) | mg/kg | 0.064 | 0.060 |
Cadmium (Cd) | mg/kg | 0.025 | 0.027 |
Arsenic (As) | mg/kg | 0.024 | 0.018 |
Component | Unit | Content | |
---|---|---|---|
Day “0” | Day 15 | ||
Harmful Substances and Pollutants | |||
PAHs | mg/kg | <0.020 | <0.020 |
PCBs | mg/kg | <0.035 | <0.035 |
Mycotoxins * | |||
Aflatoxins | mg/kg | <0.003 | <0.003 |
Fumonisins | mg/kg | <0.030 | <0.030 |
Zearalenone | mg/kg | <0.030 | <0.030 |
T-2/HT-2 toxin | µg/kg | <20 | <20 |
Deoxynivalenol | mg/kg | <0.020 | <0.020 |
Ochratoxin A | mg/kg | <0.001 | <0.001 |
Phenolic Compounds | Day “0” | SSF in Laboratory Jars | SSF in Tray Bioreactor | p *** | ||||
---|---|---|---|---|---|---|---|---|
Co (µg/gdb) * | Ci,max. (µg/gdb) * | p ** | tSSF (d) | Ci,max. (µg/gdb) * | p ** | tSSF (d) | ||
Phenolic acid (hydroxybenzoic acids) | ||||||||
GA | 307.20 ± 3.10 | 447.88 ± 33.15 | 0.0149 | 4. | 490.77 ± 15.31 | 0.0033 | 4. | 0.1117 |
EA | 208.44 ± 4.42 | 235.50 ± 6.27 | 0.0483 | 3. | 233.49 ± 1.62 | 0.0188 | 10. | 0.6183 |
p-HBA | 6.07 ± 0.44 | 14.30 ± 0.79 | 0.0006 | 4. | 11.79 ± 0.17 | 0.0008 | 3. | 0.0057 |
SA | 236.63 ± 1.28 | 424.04 ± 4.96 | 0.0004 | 5. | 282.00 ± 18.34 | 0.0441 | 1. | 0.0002 |
VA | 80.81 ± 1.31 | 97.49 ± 0.79 | 0.0053 | 2. | 93.68 ± 6.57 | 0.0514 | 1. | 0.3749 |
3,4-DHBA | 111.51 ± 2.17 | 234.14 ± 9.27 | 0.0029 | 10. | 194.24 ± 3.78 | 0.0017 | 4. | 0.0023 |
Phenolic acid (hydroxycinnamic acids) | ||||||||
p-CoA | 8.76 ± 0.70 | 9.65 ± 0.55 | 0.0098 | 4. | 10.23 ± 0.17 | 0.1000 | 4. | 0.1544 |
CAF | 13.12 ± 0.46 | 15.07 ± 0.17 | 0.0070 | 1. | 17.14 ± 0.99 | 0.0058 | 1. | 0.0235 |
Flavan-3-ol | ||||||||
EPG | 319.26 ± 3.39 | 366.73 ± 5.08 | 0.0004 | 1. | 453.49 ± 15.62 | 0.0028 | 1. | 0.0008 |
Flavonol | ||||||||
QU | 403.10 ± 9.04 | 657.79 ± 13.33 | 0.0001 | 15. | 714.91 ± 15.92 | 0.0021 | 10. | 0.0089 |
Stilbene | ||||||||
RES | 30.40 ± 0.69 | 30.63 ± 0.37 | 0.7370 | 3. | 76.19 ± 0.41 | 0.0000 | 15. | 0.0000 |
tSSF (d) | Hydrolytic Enzymes | Lignolytic Enzymes * | |||||
---|---|---|---|---|---|---|---|
β-Glucosidase (U/gdb) | Xylanase (U/gdb) | Cellulase (U/gdb) | Invertase (U/gdb) | Laccase (U/gdb) | MnP (U/gdb) | LiP (U/gdb) | |
Laboratory jars | |||||||
1. | 0.421 | 25.517 | 0.234 | n.d. | 0.005 | n.d. | 0.013 |
5. | 0.208 | 62.964 | 0.675 | n.d. | 0.001 | 0.001 | 0.006 |
10. | 0.315 | 40.054 | n.d. | 8.198 | 0.001 | 0.005 | 0.039 |
15. | 0.347 | 33.181 | 1.020 | 6.316 | 0.002 | n.d. | 0.040 |
Tray bioreactor | |||||||
1. | 0.290 | 9.271 | 0.293 | 6.135 | 0.005 | n.d. | 0.036 |
5. | 0.533 | 17.684 | 0.685 | 2.700 | 0.009 | n.d. | 0.026 |
10. | 0.440 | 46.133 | 0.666 | 10.706 | 0.071 | 0.018 | 0.069 |
15. | 0.430 | 47.673 | 0.523 | 7.344 | 0.072 | 0.018 | 0.074 |
Phenolic Compounds * | Hidrolytic Enzymes | Lignolytic Enzymes ** | |||||
---|---|---|---|---|---|---|---|
β-Glucosidase | Xylanase | Cellulase | Invertase | Laccase | MnP | LiP | |
HBA | −0.433 | 0.555 | −0.565 | −0.552 | −0.233 | 0.188 | −0.739 |
HCA | 0.149 | 0.014 | −0.579 | −0.755 | 0.404 | −0.181 | −0.790 |
F3L | 0.116 | 0.051 | −0.095 | −0.970 | 0.474 | −0.643 | −0.919 |
FL | 0.192 | −0.323 | 0.717 | 0.533 | 0.014 | −0.205 | 0.687 |
PCD | −0.476 | 0.618 | −0.225 | −0.810 | −0.163 | −0.201 | −0.937 |
ST | −0.105 | 0.273 | −0.274 | −0.923 | 0.236 | −0.398 | −0.962 |
TP | −0.331 | 0.487 | −0.154 | −0.913 | 0.019 | −0.379 | −0.987 |
Phenolic Compounds * | Hidrolytic Enzymes | Lignolytic Enzymes ** | |||||
---|---|---|---|---|---|---|---|
β-Glucosidase | Xylanase | Cellulase | Invertase | Laccase | MnP | LiP | |
HBA | −0.494 | −0.854 | −0.472 | −0.257 | −0.801 | −0.790 | −0.735 |
HCA | −0.349 | −0.966 | −0.431 | −0.534 | −0.943 | −0.937 | −0.897 |
F3L | −0.235 | −0.994 | −0.387 | −0.700 | −0.992 | −0.989 | −0.961 |
FL | 0.162 | 0.240 | 0.477 | 0.570 | 0.253 | 0.238 | 0.161 |
PCD | 0.638 | −0.532 | 0.472 | −0.781 | −0.635 | −0.669 | −0.790 |
ST | 0.203 | 0.917 | 0.253 | 0.508 | 0.908 | 0.910 | 0.903 |
TP | 0.217 | −0.792 | 0.133 | −0.643 | −0.838 | −0.857 | −0.922 |
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Šelo, G.; Planinić, M.; Tišma, M.; Martinović, J.; Perković, G.; Bucić-Kojić, A. Bioconversion of Grape Pomace with Rhizopus oryzae under Solid-State Conditions: Changes in the Chemical Composition and Profile of Phenolic Compounds. Microorganisms 2023, 11, 956. https://doi.org/10.3390/microorganisms11040956
Šelo G, Planinić M, Tišma M, Martinović J, Perković G, Bucić-Kojić A. Bioconversion of Grape Pomace with Rhizopus oryzae under Solid-State Conditions: Changes in the Chemical Composition and Profile of Phenolic Compounds. Microorganisms. 2023; 11(4):956. https://doi.org/10.3390/microorganisms11040956
Chicago/Turabian StyleŠelo, Gordana, Mirela Planinić, Marina Tišma, Josipa Martinović, Gabriela Perković, and Ana Bucić-Kojić. 2023. "Bioconversion of Grape Pomace with Rhizopus oryzae under Solid-State Conditions: Changes in the Chemical Composition and Profile of Phenolic Compounds" Microorganisms 11, no. 4: 956. https://doi.org/10.3390/microorganisms11040956
APA StyleŠelo, G., Planinić, M., Tišma, M., Martinović, J., Perković, G., & Bucić-Kojić, A. (2023). Bioconversion of Grape Pomace with Rhizopus oryzae under Solid-State Conditions: Changes in the Chemical Composition and Profile of Phenolic Compounds. Microorganisms, 11(4), 956. https://doi.org/10.3390/microorganisms11040956