This study investigates the effects of different crude protein (CP) levels on growth performance, serum biochemistry, organ indices, intestinal morphology, colonic volatile fatty acids, and gut microbiota in Ningxiang finishing pigs. Ninety-six pigs (53.20 ± 0.53 kg) were randomly assigned to three dietary treatments: high-protein (HP, 15.56% CP), medium-protein (MP, 12.94% CP), and low-protein (LP, 10.31% CP), with four replicate pens per treatment and eight pigs per pen. Results showed that dietary CP levels had no significant effects on growth performance. However, the LP diet significantly reduced serum urea nitrogen, liver weight, and relative liver weight (p < 0.05). Additionally, jejunal crypt depth showed a linear decrease in response to graded reductions in dietary CP levels (Linear, p < 0.05). The LP diet significantly decreased the contents of isobutyric, isovaleric, and branched-chain fatty acids in colonic fermentation products (p < 0.05). Furthermore, 16S rRNA sequencing revealed that the relative abundances of Terrisporobacter, Marvinbryantia, Turicibacter, Lachnospiraceae_AC2044_group, unclassified_f_Peptostreptococcaceae, norank_f_Eubacter_coprostanoligenes_group, Lachnospiraceae_UCG-007, and UCG-009 were significantly higher in the LP group (p < 0.05). Spearman correlation analysis indicated that isobutyric acid and isovaleric acid were negatively correlated with Lactobacillus and positively correlated with Streptococcus. In conclusion, the LP diet improved colonic microbiota composition while maintaining growth performance in Ningxiang finishing pigs. These results advance our understanding of protein nutrition in indigenous fat-type pig breeds, providing a theoretical foundation for optimizing dietary formulations specifically in Ningxiang pigs.
| [1] |
Y. Wang, J. Zhou, G. Wang, S. Cai, X. Zeng, and S. Qiao, “Advances in Low-Protein Diets for Swine,” Journal of Animal Science and Biotechnology9, no. 1 (2018): 60, https://doi.org/10.1186/s40104-018-0276-7.
|
| [2] |
Y. Zhao, G. Tian, D. Chen, et al., “Effect of Different Dietary Protein Levels and Amino Acids Supplementation Patterns on Growth Performance, Carcass Characteristics and Nitrogen Excretion in Growing-Finishing Pigs,” Journal of Animal Science and Biotechnology10, no. 1 (2019): 75, https://doi.org/10.1186/s40104-019-0381-2.
|
| [3] |
V. T. Rist, E. Weiss, M. Eklund, and R. Mosenthin, “Impact of Dietary Protein on Microbiota Composition and Activity in the Gastrointestinal Tract of Piglets in Relation to Gut Health: A Review,” Animal7, no. 7 (2013): 1067-1078, https://doi.org/10.1017/S1751731113000062.
|
| [4] |
S. Liu and Z. Fan, “Effects of Dietary Protein Restriction on Colonic Microbiota of Finishing Pigs,” Animals (Basel)13, no. 1 (2022): 9, https://doi.org/10.3390/ani13010009.
|
| [5] |
R. Liu, J. He, X. Ji, W. Zheng, and W. Yao, “A Moderate Reduction of Dietary Crude Protein Provide Comparable Growth Performance and Improve Metabolism via Changing Intestinal Microbiota in Sushan Nursery Pigs,” Animals (Basel)11, no. 4 (2021): 1166, https://doi.org/10.3390/ani11041166.
|
| [6] |
M. Wang, H. Sun, and Z. Xu, “Analysis of Blueberry Plant Rhizosphere Bacterial Diversity and Selection of Plant Growth Promoting Rhizobacteria,” Current Microbiology79, no. 11 (2022): 331, https://doi.org/10.1007/s00284-022-03031-z.
|
| [7] |
Y. Wang, J. Chen, Y. Ji, X. Lin, and Y. Zhao, “Effect of Betaine Diet on Growth Performance, Carcass Quality and Fat Deposition in Finishing Ningxiang Pigs,” Animals (Basel)11, no. 12 (2021): 3408, https://doi.org/10.3390/ani11123408.
|
| [8] |
E. Zong, P. Huang, W. Zhang, et al., “The Effects of Dietary Sulfur Amino Acids on Growth Performance, Intestinal Morphology, Enzyme Activity, and Nutrient Transporters in Weaning Piglets,” Journal of Animal Science96, no. 3 (2018): 1130-1139, https://doi.org/10.1093/jas/skx003.
|
| [9] |
A. Sczesnak, N. Segata, X. Qin, et al., “The Genome of Th17 Cell-Inducing Segmented Filamentous Bacteria Reveals Extensive Auxotrophy and Adaptations to the Intestinal Environment,” Cell Host & Microbe10, no. 3 (2011): 260-272, https://doi.org/10.1016/j.chom.2011.08.005.
|
| [10] |
Y. Li, X. Lu, H. Wu, et al., “The Effect of Dietary Supplementation of Low Crude Protein on Intestinal Morphology in Pigs,” Research in Veterinary Science122 (2019): 15-21, https://doi.org/10.1016/j.rvsc.2018.11.013.
|
| [11] |
P. Fan, P. Liu, P. Song, X. Chen, and X. Ma, “Moderate Dietary Protein Restriction Alters the Composition of Gut Microbiota and Improves Ileal Barrier Function in Adult Pig Model,” Scientific Reports7, no. 1 (2017): 43412, https://doi.org/10.1038/srep43412.
|
| [12] |
M. Saresella, L. Mendozzi, V. Rossi, et al., “Immunological and Clinical Effect of Diet Modulation of the Gut Microbiome in Multiple Sclerosis Patients: A Pilot Study,” Frontiers in Immunology8 (2017): 1391, https://doi.org/10.3389/fimmu.2017.01391.
|
| [13] |
L. Lei, Z. Wang, J. Li, et al., “Comparative Microbial Profiles of Colonic Digesta Between Ningxiang Pig and Large White Pig,” Animals (Basel)11, no. 7 (2021): 1862, https://doi.org/10.3390/ani11071862.
|
| [14] |
E. D. Sonnenburg, S. A. Smits, M. Tikhonov, S. K. Higginbottom, N. S. Wingreen, and J. L. Sonnenburg, “Diet-Induced Extinctions in the Gut Microbiota Compound Over Generations,” Nature529, no. 7585 (2016): 212-215, https://doi.org/10.1038/nature16504.
|
| [15] |
D. Wang, G. Chen, L. Song, et al., “Effects of Dietary Protein Levels on Bamei Pig Intestinal Colony Compositional Traits,” BioMed Research International2020, no. 1 (2020): 2610431, https://doi.org/10.1155/2020/2610431.
|
| [16] |
C. Zhu, J. Yang, Q. Wu, et al., “Low Protein Diet Improves Meat Quality and Modulates the Composition of Gut Microbiota in Finishing Pigs,” Frontiers in Veterinary Science9 (2022): 843957, https://doi.org/10.3389/fvets.2022.843957.
|
| [17] |
Y. Liu, M. A. K. Azad, X. Zhao, and X. Kong, “Crude Protein Content in Diets Associated With Intestinal Microbiome and Metabolome Alteration in Huanjiang Mini-Pigs During Different Growth Stages,” Frontiers in Microbiology15 (2024): 1398919, https://doi.org/10.3389/fmicb.2024.1398919.
|
| [18] |
Y. Zhao, G. Tian, D. Chen, et al., “Dietary Protein Levels and Amino Acid Supplementation Patterns Alter the Composition and Functions of Colonic Microbiota in Pigs,” Animal Nutrition6, no. 2 (2020): 143-151, https://doi.org/10.1016/j.aninu.2020.02.005.
|
| [19] |
C. M. Nyachoti, F. O. Omogbenigun, M. Rademacher, and G. Blank, “Performance Responses and Indicators of Gastrointestinal Health in Early-Weaned Pigs Fed Low-Protein Amino Acid-Supplemented Diets,” Journal of Animal Science84, no. 1 (2006): 125-134, https://doi.org/10.2527/2006.841125x.
|
| [20] |
X. Zeng, Y. Yang, J. Wang, et al., “Dietary Butyrate, Lauric Acid and Stearic Acid Improve Gut Morphology and Epithelial Cell Turnover in Weaned Piglets,” Animal Nutrition11 (2022): 276-282, https://doi.org/10.1016/j.aninu.2022.07.012.
|
| [21] |
Q. Deng, X. Tan, H. Wang, et al., “Changes in Cecal Morphology, Cell Proliferation, Antioxidant Enzyme, Volatile Fatty Acids, Lipopolysaccharide, and Cytokines in Piglets During the Postweaning Period,” Journal of Animal Science98, no. 3 (2020): skaa046, https://doi.org/10.1093/jas/skaa046.
|
| [22] |
Z. Wang, X. Zeng, C. Zhang, et al., “Higher Niacin Intakes Improve the Lean Meat Rate of Ningxiang Pigs by Regulating Lipid Metabolism and Gut Microbiota,” Frontiers in Nutrition9 (2022): 959039, https://doi.org/10.3389/fnut.2022.959039.
|
| [23] |
J.-Y. Dourmad and C. Jondreville, “Impact of Nutrition on Nitrogen, Phosphorus, Cu and Zn in Pig Manure, and on Emissions of Ammonia and Odours,” Livestock Science112, no. 3 (2007): 192-198, https://doi.org/10.1016/j.livsci.2007.09.002.
|
| [24] |
E. T. Hayes, A. B. Leek, T. P. Curran, et al., “The Influence of Diet Crude Protein Level on Odour and Ammonia Emissions From Finishing Pig Houses,” Bioresource Technology91, no. 3 (2004): 309-315, https://doi.org/10.1016/s0960-8524(03)00184-6.
|
| [25] |
A. Prandini, S. Sigolo, M. Morlacchini, E. Grilli, and L. Fiorentini, “Microencapsulated Lysine and Low-Protein Diets: Effects on Performance, Carcass Characteristics and Nitrogen Excretion in Heavy Growing-Finishing Pigs,” Journal of Animal Science91, no. 9 (2013): 4226-4234, https://doi.org/10.2527/jas.2013-6412.
|
| [26] |
D. Wang, G. Chen, W. Li, M. Chai, H. Zhang, and Y. Su, “Effects of Low Protein Diet on Production Performance and Intestinal Microbial Composition in Pigs,” Veterinary Sciences10, no. 11 (2023): 655, https://doi.org/10.3390/vetsci10110655.
|
| [27] |
E. Trefts, M. Gannon, and D. H. Wasserman, “The Liver,” Current Biology27, no. 21 (2017): R1147-R1151, https://doi.org/10.1016/j.cub.2017.09.019.
|
| [28] |
J. Simek, V. A. Shkurupy, G. N. Shorina, N. P. Bgatova, Z. Cervinkova, and M. Holecek, “Effect of Long-Term Administration of a High Protein or Low Protein Diet on Rat Liver. Morphological and Biochemical Findings,” Physiologia Bohemoslovaca35, no. 2 (1986): 127-133, https://doi.org/10.1007/BF00582960.
|
| [29] |
B. J. Kerr, F. K. McKeith, and R. A. Easter, “Effect on Performance and Carcass Characteristics of Nursery to Finisher Pigs Fed Reduced Crude Protein, Amino Acid-Supplemented Diets,” Journal of Animal Science73, no. 2 (1995): 433-440, https://doi.org/10.2527/1995.732433x.
|
| [30] |
X. Peng, L. Hu, Y. Liu, et al., “Effects of Low-Protein Diets Supplemented With Indispensable Amino Acids on Growth Performance, Intestinal Morphology and Immunological Parameters in 13 to 35 kg Pigs,” Animal10, no. 11 (2016): 1812-1820, https://doi.org/10.1017/S1751731116000999.
|
| [31] |
J. Lee, J. C. Gonzalez-Vega, J. K. Htoo, C. Yang, and C. M. Nyachoti, “Effects of Dietary Protein Content and Crystalline Amino Acid Supplementation Patterns on Growth Performance, Intestinal Histomorphology, and Immune Response in Weaned Pigs Raised Under Different Sanitary Conditions,” Journal of Animal Science100, no. 10 (2022): skac285, https://doi.org/10.1093/jas/skac285.
|
| [32] |
L. Qin, W. Ji, J. Wang, B. Li, J. Hu, and X. Wu, “Effects of Dietary Supplementation With Yeast Glycoprotein on Growth Performance, Intestinal Mucosal Morphology, Immune Response and Colonic Microbiota in Weaned Piglets,” Food & Function10, no. 5 (2019): 2359-2371, https://doi.org/10.1039/c8fo02327a.
|
| [33] |
X. Ding, H. Li, Z. Wen, et al., “Effects of Fermented Tea Residue on Fattening Performance, Meat Quality, Digestive Performance, Serum Antioxidant Capacity, and Intestinal Morphology in Fatteners,” Animals (Basel)10, no. 2 (2020): 185, https://doi.org/10.3390/ani10020185.
|
| [34] |
H. Huan, J. Bai, W. Zhou, et al., “Effects of Antimicrobial Peptides on Serum Biochemical Indices, Intestinal Mucosa Morphology and Relative Expression Level of Tight Junction Protein Gene of Jejunum of Piglets,” Chinese Journal of Animal Nutrition27, no. 12 (2015): 3797-3804, https://doi10.3969/j.issn.1006-267x.
|
| [35] |
X. Zhan, L. Hou, Z. He, et al., “Effect of Miscellaneous Meals Replacing Soybean Meal in Feed on Growth Performance, Serum Biochemical Parameters, and Microbiota Composition of 25-50 kg Growing Pigs,” Animals (Basel)14, no. 9 (2024): 1354, https://doi.org/10.3390/ani14091354.
|
| [36] |
N. Ma, Y. Tian, Y. Wu, and X. Ma, “Contributions of the Interaction Between Dietary Protein and Gut Microbiota to Intestinal Health,” Current Protein & Peptide Science18, no. 8 (2017): 795-808, https://doi.org/10.2174/1389203718666170216153505.
|
| [37] |
C. Kaewtapee, K. Burbach, G. Tomforde, et al., “Effect of Bacillus subtilis and Bacillus licheniformis Supplementation in Diets With Low- and High-Protein Content on Ileal Crude Protein and Amino Acid Digestibility and Intestinal Microbiota Composition of Growing Pigs,” Journal of Animal Science and Biotechnology8, no. 1 (2017): 37, https://doi.org/10.1186/s40104-017-0168-2.
|
| [38] |
S. Namted, K. Poungpong, W. Loongyai, C. Rakangthong, and C. Bunchasak, “Dietary Autolysed Yeast Modulates Blood Profiles, Small Intestinal Morphology and Caecal Microbiota of Weaning Pigs,” Animal16, no. 11 (2022): 100660, https://doi.org/10.1016/j.animal.2022.100660.
|
| [39] |
R. Hu, F. Zeng, L. Wu, et al., “Fermented Carrot Juice Attenuates Type 2 Diabetes by Mediating Gut Microbiota in Rats,” Food & Function10, no. 5 (2019): 2935-2946, https://doi.org/10.1039/c9fo00475k.
|
| [40] |
J. Zhou, Y. Wang, L. Wang, et al., “Compromised Hindgut Microbial Digestion, rather Than Chemical Digestion in the Foregut, Leads to Decreased Nutrient Digestibility in Pigs Fed Low-Protein Diets,” Nutrients14, no. 14 (2022): 2793, https://doi.org/10.3390/nu14142793.
|
| [41] |
K. L. Gomes Carvalho Alves, Y. T. Granja-Salcedo, J. D. Messana, et al., “Rumen Bacterial Diversity in Relation to Nitrogen Retention in Beef Cattle,” Anaerobe67 (2021): 102316, https://doi.org/10.1016/j.anaerobe.2020.102316.
|
| [42] |
Y. Leng, M. Yi, J. Fan, Y. Bai, Q. Ge, and G. Yao, “Effects of Acute Intra-Abdominal Hypertension on Multiple Intestinal Barrier Functions in Rats,” Scientific Reports6, no. 1 (2016): 22814, https://doi.org/10.1038/srep22814.
|
| [43] |
L. Li, K. Buhman, P. Hartman, and D. Beitz, “Hypocholesterolemic Effect of Eubacterium Coprostanoligenes Atcc 51222 in Rabbits,” Letters in Applied Microbiology20, no. 3 (1995): 137-140, https://doi.org/10.1111/j.1472-765X.1995.tb00410.x.
|
| [44] |
G. L. Hold, M. C. Costa, L. G. Arroyo, et al., “Comparison of the Fecal Microbiota of Healthy Horses and Horses With Colitis by High Throughput Sequencing of the v3–v5 Region of the 16s rrna Gene,” PLoS One7, no. 7 (2012): e41484, https://doi.org/10.1371/journal.pone.0041484.
|
| [45] |
N. Kaku, N. Matsumoto, D. Sasaki, et al., “Effect of Probiotics on Gut Microbiome in Patients With Administration of Surgical Antibiotic Prophylaxis: A Randomized Controlled Study,” Journal of Infection and Chemotherapy26, no. 8 (2020): 795-801, https://doi.org/10.1016/j.jiac.2020.03.008.
|
| [46] |
L. Jin, K. Li, Z. Li, et al., “Investigation into Critical Gut Microbes Influencing Intramuscular Fat Deposition in Min Pigs,” Animals14 (2024): 21, https://doi.org/10.3390/ani14213123.
|
| [47] |
X. Lai, S. Liu, J. Miao, et al., “Eubacterium Siraeum Suppresses Fat Deposition via Decreasing the Tyrosine-Mediated pi3k/akt Signaling Pathway in High-Fat Diet-Induced Obesity,” Microbiome12, no. 1 (2024): 223, https://doi.org/10.1186/s40168-024-01944-4.
|
| [48] |
J. K. Htoo, B. A. Araiza, W. C. Sauer, et al., “Effect of Dietary Protein Content on Ileal Amino Acid Digestibility, Growth Performance, and Formation of Microbial Metabolites in Ileal and Cecal Digesta of Early-Weaned Pigs,” Journal of Animal Science85, no. 12 (2007): 3303-3312, https://doi.org/10.2527/jas.2007-0105.
|
| [49] |
L. Zhou, L. Fang, Y. Sun, Y. Su, and W. Zhu, “Effects of the Dietary Protein Level on the Microbial Composition and Metabolomic Profile in the Hindgut of the Pig,” Anaerobe38 (2016): 61-69, https://doi.org/10.1016/j.anaerobe.2015.12.009.
|
| [50] |
S. Cho, O. Hwang, and S. Park, “Effect of Dietary Protein Levels on Composition of Odorous Compounds and Bacterial Ecology in Pig Manure,” Asian-Australasian Journal of Animal Sciences28, no. 9 (2015): 1362-1370, https://doi.org/10.5713/ajas.15.0078.
|
| [51] |
S. Spring, H. Premathilake, C. Bradway, et al., “Effect of Very Low-Protein Diets Supplemented With Branched-Chain Amino Acids on Energy Balance, Plasma Metabolomics and Fecal Microbiome of Pigs,” Scientific Reports10, no. 1 (2020): 15859, https://doi.org/10.1038/s41598-020-72816-8.
|
| [52] |
M. R. Obradovic, M. Segura, J. Segales, and M. Gottschalk, “Review of the Speculative Role of Co-Infections in Streptococcus Suis-Associated Diseases in Pigs,” Veterinary Research52, no. 1 (2021): 49, https://doi.org/10.1186/s13567-021-00918-w.
|
| [53] |
M. R. Davies, M. T. Holden, P. Coupland, et al., “Emergence of Scarlet Fever Streptococcus Pyogenes emm12 Clones in Hong Kong Is Associated With Toxin Acquisition and Multidrug Resistance,” Nature Genetics47, no. 1 (2015): 84-87, https://doi.org/10.1038/ng.3147.
|
| [54] |
M. P. Mokoena, “Lactic Acid Bacteria and Their Bacteriocins: Classification, Biosynthesis and Applications Against Uropathogens: A Mini-Review,” Molecules22, no. 8 (2017): 1255, https://doi.org/10.3390/molecules22081255.
|
| [55] |
P. Alvarez-Sieiro, M. Montalban-Lopez, D. Mu, and O. P. Kuipers, “Bacteriocins of Lactic Acid Bacteria: Extending the Family,” Applied Microbiology and Biotechnology100, no. 7 (2016): 2939-2951, https://doi.org/10.1007/s00253-016-7343-9.
|
| [56] |
V. T. Rist, E. Weiss, N. Sauer, R. Mosenthin, and M. Eklund, “Effect of Dietary Protein Supply Originating From Soybean Meal or Casein on the Intestinal Microbiota of Piglets,” Anaerobe25 (2014): 72-79, https://doi.org/10.1016/j.anaerobe.2013.10.003.
|
| [57] |
H. Wang, J. Shen, C. Mu, K. Gao, Y. Pi, and W. Zhu, “Low Crude Protein Diets Supplemented With Casein Hydrolysate Enhance the Intestinal Barrier Function and Decrease the Pro-Inflammatory Cytokine Expression in the Small Intestine of Pigs,” Animal Nutrition7, no. 3 (2021): 770-778, https://doi.org/10.1016/j.aninu.2021.03.003.
|
| [58] |
J. Gao, Z. Liu, C. Wang, L. Ma, Y. Chen, and T. Li, “Effects of Dietary Protein Level on the Microbial Composition and Metabolomic Profile in Postweaning Piglets,” Oxidative Medicine and Cellular Longevity2022, no. 1 (2022): 3355687, https://doi.org/10.1155/2022/3355687.
|
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