Long-Term Dietary Fish Meal Substitution with the Black Soldier Fly Larval Meal Modifies the Caecal Microbiota and Microbial Pathway in Laying Hens
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Diets, Animals, and Sampling
2.2. Quantification of Free Amino Acid in Liver
2.3. Quantification of Fatty Acid Concentration in Liver
2.4. Measurement of Plasma Biochemical Parameter
2.5. Disaccharidase Activity Test in Intestinal Mucosa
2.6. Intestinal Morphological Analysis
2.7. 16S rRNA Gene Amplicon Sequencing and Taxonomic Analysis
2.8. Determination of Short-Chain Fatty Acid in Caecal Content
2.9. Prediction of Microbial Functional Abundance and Metabolic Pathway Analysis
2.10. Statistical Analysis
3. Results
3.1. Free Amino Acids in the Liver
3.2. Fatty Acid Concentration in the Liver
3.3. Plasma Biochemical Parameters
3.4. Disaccharidase Activities in Intestinal Mucosa
3.5. Intestinal Morphology
3.6. Caecal Microbiota
3.7. SCFAs Concentrations in Caecal Content
3.8. Microbial Functional Abundance Prediction and Metabolic Pathway
4. Discussion
5. 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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Amino Acids (mmol/L) | Diets | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
Alanine | 1.694 ± 0.076 | 1.648 ± 0.084 | 1.865 ± 0.133 | 0.527 |
Arginine | 2.223 ± 0.130 | 2.045 ± 0.085 | 2.724 ± 0.238 | 0.123 |
Asparagine | 0.363 ± 0.029 | 0.342 ± 0.031 | 0.491 ± 0.053 | 0.059 |
Aspartate | 1.749 ± 0.105 bc | 1.610 ± 0.080 c | 2.275 ± 0.176 a | 0.023 |
Glutamate | 2.486 ± 0.143 | 2.293 ± 0.128 | 2.868 ± 0.237 | 0.145 |
Glutamine | 2.752 ± 0.183 | 2.543 ± 0.149 | 3.317 ± 0.316 | 0.181 |
Glycine | 0.757 ± 0.039 | 0.760 ± 0.041 | 0.922 ± 0.072 | 0.171 |
Histidine | 5.480 ± 0.274 | 5.178 ± 0.270 | 5.809 ± 0.491 | 0.783 |
Isoleucine | 1.139 ± 0.068 | 1.066 ± 0.046 | 1.435 ± 0.200 | 0.070 |
Leucine | 1.250 ± 0.073 | 1.179 ± 0.049 | 1.582 ± 0.132 | 0.072 |
Lysine | 3.126 ± 0.184 | 3.103 ± 0.152 | 4.090 ± 0.365 | 0.145 |
Methionine | 2.684 ± 0.146 | 2.495 ± 0.109 | 3.378 ± 0.278 | 0.052 |
Phenylalanine | 1.348 ± 0.077 | 1.229 ± 0.058 | 1.436 ± 0.112 | 0.450 |
Proline | 2.399 ± 0.130 | 2.287 ± 0.105 | 2.865 ± 0.245 | 0.333 |
Serine | 5.326 ± 0.232 | 4.754 ± 0.221 | 5.539 ± 0.377 | 0.611 |
Threonine | 1.473 ± 0.082 | 1.341 ± 0.062 | 1.785 ± 0.146 | 0.065 |
Tryptophan | 0.192 ± 0.010 | 0.180 ± 0.009 | 0.191 ± 0.012 | 0.950 |
Tyrosine | 1.482 ± 0.069 | 1.350 ± 0.063 | 1.487 ± 0.117 | 0.418 |
Valine | 2.504 ± 0.137 | 2.250 ± 0.102 | 2.598 ± 0.219 | 0.458 |
Fatty Acids (mg/g) | Diets | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
Linoleic acid (C22: 2(n-6)) | 0.80 ± 0.16 | 0.76 ± 0.09 | 0.84 ± 0.15 | 0.826 |
Oleic acid (C22: 0) | 5.01 ± 0.73 | 6.27 ± 1.07 | 5.85 ± 1.02 | 0.665 |
Palmitic acid (C16: 0) | 1.32 ± 0.21 | 1.84 ± 0.45 | 1.54 ± 0.26 | 0.693 |
Stearic acid (C18: 0) | 0.77 ± 0.17 | 0.92 ± 0.18 | 0.83 ± 0.13 | 0.377 |
Parameters | Diets | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
ALP (IU/L) | 322.86 ± 42.82 | 365.23 ± 59.12 | 281.73 ± 25.27 | 0.806 |
GOT (IU/L) | 112.14 ± 10.86 | 144.62 ± 11.71 | 123.20 ± 9.88 | 0.069 |
GGT (IU/L) | 17.86 ± 1.33 | 19.38 ± 1.75 | 18.80 ± 1.26 | 0.762 |
LDH (IU/L) | 214.86 ± 20.76 | 336.46 ± 46.00 | 307.60 ± 44.73 | 0.138 |
HDL-c (mg/dL) | 22.79 ± 7.05 | 20.67 ± 9.04 | 19.57 ± 8.76 | 0.305 |
T-cho (mg/dL) | 104.00 ± 27.30 | 100.33 ± 26.92 | 103.33 ± 27.40 | 0.901 |
Ca (mg/dL) | 22.73 ± 1.40 | 25.75 ± 1.38 | 23.85 ± 1.55 | 0.160 |
Mg (mg/dL) | 2.80 ± 0.18 | 3.28 ± 0.22 | 2.97 ± 0.20 | 0.264 |
IP (mg/dL) | 7.30 ± 0.80 | 8.11 ± 0.78 | 7.49 ± 0.79 | 0.513 |
IgG (mg/mL) | 7.43 ± 1.37 | 7.56 ± 1.62 | 9.69 ± 1.27 | 0.479 |
TNF-α (pg/mL) | 148.78 ± 37.49 | 134.87 ± 54.60 | 134.94 ± 43.69 | 0.834 |
Disaccharidase Activities (mU/mg) | Diets | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
Jejunum | ||||
Maltase activity | 0.949 ± 0.060 | 0.845 ± 0.058 | 0.868 ± 0.079 | 0.971 |
Sucrase activity | 0.678 ± 0.028 | 0.688 ± 0.033 | 0.687 ± 0.032 | 0.344 |
Ileum | ||||
Maltase activity | 0.397 ± 0.030 ab | 0.318 ± 0.026 b | 0.429 ± 0.032 a | 0.025 |
Sucrase activity | 0.165 ± 0.042 | 0.111 ± 0.025 | 0.240 ± 0.078 | 0.218 |
Intestines | Diets | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
Duodenum | ||||
Villi height (µm) | 1082.95 ± 51.08 | 1031.17 ± 51.81 | 1040.39 ± 26.87 | 0.803 |
Crypt depth (µm) | 168.77 ± 5.96 | 174.62 ± 5.43 | 176.09 ± 7.14 | 0.681 |
Villi/Crypt | 6.57 ± 0.44 | 5.95 ± 0.30 | 6.09 ± 0.35 | 0.462 |
Goblet cell density (103/mm2) | 2.21 ± 0.16 | 1.86 ± 0.07 | 1.78 ± 0.08 | 0.088 |
Jejunum | ||||
Villi height (µm) | 793.47 ± 53.03 | 771.34 ± 37.3 | 817.66 ± 44.70 | 0.773 |
Crypt depth (µm) | 104.52 ± 4.80 | 113.1 ± 4.46 | 108.38 ± 4.59 | 0.320 |
Villi/Crypt | 7.63 ± 0.44 | 6.89 ± 0.32 | 7.62 ± 0.43 | 0.337 |
Goblet cell density (103/mm2) | 2.02 ± 0.14 | 1.62 ± 0.12 | 1.61 ± 0.17 | 0.085 |
Ileum | ||||
Villi height (µm) | 529.44 ± 24.64 | 561.27 ± 31.87 | 545.65 ± 14.03 | 0.787 |
Crypt depth (µm) | 87.45 ± 4.50 | 90.81 ± 3.96 | 93.49 ± 6.50 | 0.705 |
Villi/Crypt | 6.14 ± 0.26 | 6.20 ± 0.25 | 6.08 ± 0.31 | 0.957 |
Goblet cell density (103/mm2) | 1.78 ± 0.14 | 1.65 ± 0.13 | 1.44 ± 0.06 | 0.139 |
Pathways | Pathway Enrichment Ratio (%) | p-Value | ||
---|---|---|---|---|
C Diet | L Diet | H Diet | ||
β-glucosidase | 2.37 ± 0.10 a | 2.23 ± 0.06 ab | 2.07 ± 0.09 bc | 0.041 |
Long-chain acyl-CoA synthetase | 2.41 ± 0.10 a | 2.20 ± 0.06 ab | 2.06 ± 0.10 bc | 0.031 |
UDP glucose 6-dehydrogenase | 2.36 ± 0.09 a | 2.25 ± 0.06 ab | 2.06 ± 0.09 bc | 0.041 |
periplasmic protein TonB | 2.43 ± 0.13 a | 2.18 ± 0.08 ab | 2.05 ± 0.13 bc | 0.043 |
Bile acid: Na+ symporter, BASS family | 2.41 ± 0.12 a | 2.20 ± 0.07 ab | 2.05 ± 0.11 bc | 0.041 |
K+-stimulated pyrophosphate-energized sodium pump | 2.33 ± 0.08 a | 2.26 ± 0.05 ab | 2.08 ± 0.07 bc | 0.045 |
Carboxynorspermidine decarboxylase | 2.34 ± 0.08 a | 2.25 ± 0.06 ab | 2.08 ± 0.07 bc | 0.034 |
Saccharopine dehydrogenase | 2.33 ± 0.08 a | 2.25 ± 0.05 ab | 2.09 ± 0.07 bc | 0.050 |
Alpha-D-xyloside xylohydrolase | 2.41 ± 0.09 a | 2.17 ± 0.07 ab | 2.09 ± 0.08 bc | 0.020 |
6-pyruvoyltetrahydropterin synthase | 2.38 ± 0.10 a | 2.23 ± 0.21 ab | 2.06 ± 0.10 bc | 0.050 |
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Zhao, J.; Ban, T.; Miyawaki, H.; Hirayasu, H.; Izumo, A.; Iwase, S.-i.; Kasai, K.; Kawasaki, K. Long-Term Dietary Fish Meal Substitution with the Black Soldier Fly Larval Meal Modifies the Caecal Microbiota and Microbial Pathway in Laying Hens. Animals 2023, 13, 2629. https://doi.org/10.3390/ani13162629
Zhao J, Ban T, Miyawaki H, Hirayasu H, Izumo A, Iwase S-i, Kasai K, Kawasaki K. Long-Term Dietary Fish Meal Substitution with the Black Soldier Fly Larval Meal Modifies the Caecal Microbiota and Microbial Pathway in Laying Hens. Animals. 2023; 13(16):2629. https://doi.org/10.3390/ani13162629
Chicago/Turabian StyleZhao, Junliang, Takuma Ban, Hironori Miyawaki, Hirofumi Hirayasu, Akihisa Izumo, Shun-ichiro Iwase, Koji Kasai, and Kiyonori Kawasaki. 2023. "Long-Term Dietary Fish Meal Substitution with the Black Soldier Fly Larval Meal Modifies the Caecal Microbiota and Microbial Pathway in Laying Hens" Animals 13, no. 16: 2629. https://doi.org/10.3390/ani13162629
APA StyleZhao, J., Ban, T., Miyawaki, H., Hirayasu, H., Izumo, A., Iwase, S.-i., Kasai, K., & Kawasaki, K. (2023). Long-Term Dietary Fish Meal Substitution with the Black Soldier Fly Larval Meal Modifies the Caecal Microbiota and Microbial Pathway in Laying Hens. Animals, 13(16), 2629. https://doi.org/10.3390/ani13162629