Cultivar and Harvest Time of Almonds Affect Their Antioxidant and Nutritional Profile through Gut Microbiota Modifications
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals
2.2. Samples
2.3. Morphological Measurements
2.4. Determination of Ash, Moisture and Protein Content
2.5. In Vitro Digestion and Fermentation
2.6. Antioxidant Assays
2.6.1. Trolox Equivalent Antioxidant Capacity against ABTS Radicals (TEACABTS) Assay
2.6.2. Trolox Equivalent Antioxidant Capacity Referred to Reducing Capacity (TEACFRAP) Assay
2.6.3. Trolox Equivalent Antioxidant Capacity against DPPH Radicals (TEACDPPH) Assay
2.6.4. Folin–Ciocalteu Assay
2.7. Ultra-High Performance Liquid Chromatography (UHPLC) Analysis
2.7.1. Analysis of Phenolic Compounds
2.7.2. Analysis of SCFAs, Lactic and Succinic Acids
2.8. Microbial Genomic DNA Isolation and High Throughput Sequencing
2.9. Statistical Analyses
3. Results and Discussion
3.1. Influence of Cultivar and Harvest Time on Ash, Moisture, Protein, and Morphology of Almonds
3.2. Antioxidant Capacity of the Samples Obtained after In Vitro Digestion and Fermentation
3.2.1. Evolution of the Total Antioxidant Capacity over Harvest Time
3.2.2. Contribution of In Vitro Digestion-Fermentation Fractions to Total Antioxidant Capacity
3.3. Microbiota Community Structure Supported by Fermentation of Digested Almond Samples
3.4. Phenolic Compounds, SCFAs and Lactic and Succinic Acids Measured after In Vitro Digestion and Fermentation
3.4.1. Phenolic Compounds
3.4.2. SCFAs, Lactic and Succinic Acids
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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Cultivar | Harvest Time | Length (cm) | Width (cm) | Thickness (cm) | Ash (%) | Moisture (%) | Protein (%) |
---|---|---|---|---|---|---|---|
Guara | T1 | 2.47 ± 0.13 | 1.09 ± 0.10 a | 0.70 ± 0.09 a | 1.38 ± 0.12 a | 65.1 ± 1.10 | 11.2 ± 1.13 a |
T2 | 2.51 ± 0.13 | 1.28 ± 0.08 | 0.70 ± 0.05 a | 1.40 ± 0.21 a | 47.9 ± 0.20 | 12.8 ± 0.62 a | |
T3 | 2.41 ± 0.06 | 1.14 ± 0.14 a | 0.40 ± 0.05 | 5.55 ± 0.27 | 7.00 ± 0.10 | 24.6 ± 4.82 | |
Significance | NS | * | * | NS | * | * | |
Vairo | T1 | 2.24 ± 0.09 | 1.04 ± 0.09 | 0.56 ± 0.07 a | 1.61 ± 0.01 ab | 63.1 ± 0.6 | 14.8 ± 5.54 ab |
T2 | 2.18 ± 0.11 | 1.11 ± 0.07 | 0.55 ± 0.05 a | 1.65 ± 0.14 a | 44.7 ± 0.8 | 13.8 ± 1.03 a | |
T3 | 2.26 ± 0.10 | 1.11 ± 0.12 | 0.36 ± 0.05 | 3.63 ± 0.25 b | 6.00 ± 0.30 | 22.3 ± 0.72 b | |
Significance | NS | NS | * | NS | * | * | |
Marta | T1 | 2.34 ± 0.13 | 1.01 ± 0.12 ab | 0.73 ± 0.05 a | 1.37 ± 0.06 | 66.9 ± 1.1 a | 12.5 ± 3.28 |
T2 | 2.27 ± 0.12 | 1.10 ± 0.07 a | 0.71 ± 0.07 a | 1.64 ± 0.04 | 55.1 ± 2.00 a | 9.36 ± 2.56 | |
T3 | 2.25 ± 0.12 | 0.93 ± 0.09 b | 0.42 ± 0.06 | 4.56 ± 0.69 | 6.50 ± 0.00 | 22.6 ± 1.13 | |
Significance | NS | * | * | NS | NS | * | |
Marinada | T1 | 2.07 ± 0.12 a | 1.09 ± 0.10 ab | 0.71 ± 0.03 a | 1.14 ± 0.07 | 76.6 ± 0.30 | 6.96 ± 0.21 |
T2 | 2.28 ± 0.18 b | 1.05 ± 0.08 a | 0.49 ± 0.06 a | 1.55 ± 0.02 | 47.7 ± 1.30 | 12.8 ± 1.74 | |
T3 | 2.11 ± 0.14 ab | 1.20 ± 0.13 b | 0.69 ± 0.09 | 3.25 ± 1.08 | 8.80 ± 0.60 | 21.4 ± 1.54 | |
Significance | * | * | * | NS | NS | * | |
Marcona | T1 | 1.80 ± 0.08 | 1.20 ± 0.08 | 0.84 ± 0.05 | 1.41 ± 0.09 a | 54.6 ± 2.80 a | 10.2 ± 0.82 |
T2 | 1.70 ± 0.12 | 1.14 ± 0.11 | 0.75 ± 0.07 | 1.63 ± 0.09 a | 50.3 ± 0.50 a | 11.8 ± 1.74 | |
T3 | 1.74 ± 0.05 | 1.17 ± 0.05 | 0.62 ± 0.06 | 3.71 ± 0.15 | 9.30 ± 1.10 | 21.2 ± 5.33 | |
Significance | NS | NS | * | NS | * | * |
Guara | Vairo | Marta | Marinada | Marcona | Significance | |
---|---|---|---|---|---|---|
(+)-Catechin | 104 ± 48.0 | 97.7 ± 55.6 | 73.4 ± 53.1 | 67.7 ± 63.3 | 83.0 ± 48.2 | NS |
(-)-Epicatechin | 140 ± 65.8 ab | 90.1 ± 35.7 acd | 66.4 ± 18.9 bce | 38.2 ± 15.3 f | 49.0 ± 17.1 def | * |
(-)-Epigallocatechin | 49.9 ± 9.33 abcd | 61.6 ± 9.71 aef | 43.2 ± 14.5 begh | 33.4 ± 15.8 cgi | 52.0 ± 15.2 dfhi | * |
Ferulic acid | 0.002 ± 0 abcd | 0.005 ± 0.003 aefg | 0.002 ± 0 behi | 0.002 ± 0.001 cfhj | 0.002 ± 0 dgij | * |
Kaempferol | 0.006 ± 0.002 | 0.005 ± 0.001 | 0.006 ± 0.002 | 0.004 ± 0.001 | 0.008 ± 0.003 | NS |
Naringenin | 0.003 ± 0.001 | 0.004 ± 0 | 0.003 ± 0.001 | 0.003 ± 0.001 | 0.003 ± 0.001 | NS |
Naringin | 0.003 ± 0.002 | 0.003 ± 0.001 | 0.002 ± 0.001 | 0.002 ± 0 | 0.003 ± 0.001 | NS |
p-Coumaric acid | 0.002 ± 0.001 abcd | 0.004 ± 0.003 aefg | 0.002 ± 0.002 behi | 0.001 ± 0 cfhj | 0.006 ± 0.006 dgij | * |
Quercetin | 54.4 ± 16.2 | 61.8 ± 8.64 | 51.9 ± 10.5 | 51.8 ± 15.0 | 53.6 ± 13.8 | NS |
Rutin | 84.0 ± 11.6 abcd | 80.7 ± 7.86 aefg | 75.6 ± 5.03 behi | 76.7 ± 2.28 cfh | 81.9 ± 3.63 dgi | * |
3,4-dihydroxyphenylacetic acid | 38.4 ± 14.3 | 35.4 ± 10.3 | 31.5 ± 13.4 | 23.7 ± 13.5 | 28.7 ± 5.84 | NS |
3-(3,4-dihydroxyphenyl)propionic acid | 269 ± 106 ab | 146 ± 73.4 acde | 84.3 ± 66.7 cfg | 87.8 ± 42.0 dfh | 161 ± 95.6 begh | * |
3-(3-hydroxyphenyl)propionic acid | 21.0 ± 7.28 abcd | 4.97 ± 11.6 aefg | 9.20 ± 8.17 behi | 11.7 ± 12.8 cfhj | 19.1 ± 11.7 dgij | * |
5-(3′,4′-dihydroxyphenyl)-γ-valerolactone | 54.6 ± 57.0 ab | 183 ± 157 acde | 274 ± 115 cfg | 240 ± 113 dfh | 213 ± 134 begh | * |
Phenol | 9.45 ± 2.79 | 8.41 ± 1.72 | 9.04 ± 4.11 | 10.6 ± 4.38 | 9.79 ± 4.42 | NS |
Phloroglucinol | 207 ± 80.2 abcd | 259 ± 56.2 ae | 199 ± 34.4 befg | 168 ± 46.7 cfh | 186 ± 35.5 dgh | * |
Urolithin A | 0.022 ± 0.011 | 0.026 ± 0.009 | 0.021 ± 0.008 | 0.017 ± 0.006 | 0.025 ± 0.016 | NS |
Urolithin B | 0.002 ± 0 abc | 0.002 ± 0.001 adef | 0.001 ± 0 d | 0.002 ± 0 be | 0.004 ± 0.002 cf | * |
Total | 1055 ± 39.2 | 1027 ± 40.9 | 921 ± 113 | 814 ± 24.0 | 944 ± 24.3 | NS |
T1 | T2 | T3 | Significance | |
---|---|---|---|---|
(+)-Catechin | 97.3 ± 55.6 | 71.5 ± 53.9 | 85.6 ± 50.5 | NS |
(-)-Epicatechin | 97.3 ± 56.9 | 78.7 ± 59.2 | 53.6 ± 18.7 | NS |
(-)-Epigallocatechin | 54.1 ± 18.5 ab | 47.6 ± 13.3 ac | 40.2 ± 12.11 bc | * |
Ferulic acid | 0.003 ± 0.002 | 0.002 ± 0.001 | 0.003 ± 0.002 | NS |
Kaempferol | 0.006 ± 0.003 | 0.005 ± 0.002 | 0.007 ± 0.002 | NS |
Naringenin | 0.003 ± 0.001 a | 0.003 ± 0.001 ab | 0.004 ± 0.001 b | * |
Naringin | 0.002 ± 0.001 | 0.003 ± 0.001 | 0.003 ± 0.001 | NS |
p-Coumaric acid | 0.004 ± 0.005 | 0.002 ± 0.002 | 0.003 ± 0.002 | NS |
Quercetin | 67.9 ± 5.92 | 48.0 ± 9.78 a | 48.2 ± 10.3 a | * |
Rutin | 81.8 ± 10.0 | 81.1 ± 5.24 | 76.6 ± 4.77 | NS |
3,4-dihydroxyphenylacetic acid | 36.6 ± 12.4 | 32.6 ± 7.41 | 26.5 ± 14.7 | NS |
3-(3,4-dihydroxyphenyl)propionic acid | 162 ± 99.3 | 139 ± 70.3 | 142 ± 133 | NS |
3-(3-hydroxyphenyl)propionic acid | 16.2 ± 12.6 | 10.7 ± 8.78 | 13.6 ± 13.2 | NS |
5-(3′,4′-dihydroxyphenyl)-γ-valerolactone | 214 ± 117 | 180 ± 138 | 185 ± 163 | NS |
Phenol | 12.5 ± 2.86 | 8.77 ± 2.86 a | 7.08 ± 2.57 a | * |
Phloroglucinol | 220 ± 69.2 | 204.7 ± 47.1 | 186 ± 59.3 | NS |
Urolithin A | 0.032 ± 0.011 | 0.018 ± 0.006 a | 0.016 ± 0.005 a | * |
Urolithin B | 0.002 ± 0.002 | 0.002 ± 0.001 | 0.002 ± 0.001 | NS |
Total | 1073 ± 49.4 | 921 ± 72.1 | 863 ± 159 | NS |
Harvest Time | Acetic Acid | Propionic Acid | Butyric Acid | Lactic Acid | Succinic Acid | Total SCFAs |
---|---|---|---|---|---|---|
T1 | 12.0 ± 1.62 | 1.80 ± 0.38 ab | 0.44 ± 0.25 a | 7.13 ± 0.65 | 12.2 ± 0.22 ab | 14.3 ± 2.22 |
T2 | 12.9 ± 2.61 | 3.51 ± 2.17 ac | 0.50 ± 0.31 a | 6.89 ± 0.58 | 8.62 ± 4.67 ac | 15.6 ± 4.65 |
T3 | 14.5 ± 6.12 | 3.82 ± 3.05 bc | 2.35 ± 1.92 | 7.36 ± 1.00 | 12.2 ± 2.64 bc | 16.9 ± 10.9 |
Significance | NS | * | * | NS | * | NS |
Cultivar | Acetic acid | Propionic acid | Butyric acid | Lactic acid | Succinic acid | Total SCFAs |
Guara | 19.5 ± 5.16 abc | 6.16 ± 3.2 abcd | 2.48 ± 2.29 abcd | 6.07 ± 0.19 a | 7.50 ± 3.76 abcd | 28.2 ± 10.4 abcd |
Vairo | 12.6 ± 0.92 ade | 2.21 ± 0.57 aefg | 0.97 ± 1.00 aefg | 7.58 ± 0.10 bcd | 12.2 ± 0.62 aefg | 15.7 ± 2.42 aefg |
Marta | 12.1 ± 0.38 bd | 2.25 ± 0.44 behi | 1.22 ± 1.35 behi | 7.49 ± 0.33 bef | 12.8 ± 0.56 behi | 15.6 ± 1.46 beh |
Marinada | 11.1 ± 0.08 ce | 2.97 ± 1.94 cfhj | 0.33 ± 0.05 cfhj | 7.23 ± 0.53 ceg | 9.54 ± 5.10 cfhj | 14.4 ± 2.03 cfhi |
Marcona | 10.6 ± 0.09 | 1.63 ± 0.18 dgij | 0.48 ± 0.24 dgij | 7.26 ± 1.09 adfg | 13.0 ± 0.74 dgij | 12.7 ± 0.36 dgi |
Significance | * | * | * | * | * | * |
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Delgado-Osorio, A.; Navajas-Porras, B.; Pérez-Burillo, S.; Hinojosa-Nogueira, D.; Toledano-Marín, Á.; Pastoriza de la Cueva, S.; Paliy, O.; Rufián-Henares, J.Á. Cultivar and Harvest Time of Almonds Affect Their Antioxidant and Nutritional Profile through Gut Microbiota Modifications. Antioxidants 2024, 13, 84. https://doi.org/10.3390/antiox13010084
Delgado-Osorio A, Navajas-Porras B, Pérez-Burillo S, Hinojosa-Nogueira D, Toledano-Marín Á, Pastoriza de la Cueva S, Paliy O, Rufián-Henares JÁ. Cultivar and Harvest Time of Almonds Affect Their Antioxidant and Nutritional Profile through Gut Microbiota Modifications. Antioxidants. 2024; 13(1):84. https://doi.org/10.3390/antiox13010084
Chicago/Turabian StyleDelgado-Osorio, Adriana, Beatriz Navajas-Porras, Sergio Pérez-Burillo, Daniel Hinojosa-Nogueira, Ángela Toledano-Marín, Silvia Pastoriza de la Cueva, Oleg Paliy, and José Ángel Rufián-Henares. 2024. "Cultivar and Harvest Time of Almonds Affect Their Antioxidant and Nutritional Profile through Gut Microbiota Modifications" Antioxidants 13, no. 1: 84. https://doi.org/10.3390/antiox13010084