The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i>
The most economically important trait of the <i>Procambarus clarkii</i> is meat quality. Protein deposition is essential in muscle growth and nutritional quality formation. The effects and potential mechanisms of feed protein sources on crustaceans’ muscle protein deposition have not bee...
Saved in:
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2024-12-01
|
Series: | Microorganisms |
Subjects: | |
Online Access: | https://www.mdpi.com/2076-2607/13/1/11 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1832587903715246080 |
---|---|
author | Xiaodi Xu Xiaochuan Zheng Qunlan Zhou Cunxin Sun Aimin Wang Aimin Zhu Yuanyuan Zhang Bo Liu |
author_facet | Xiaodi Xu Xiaochuan Zheng Qunlan Zhou Cunxin Sun Aimin Wang Aimin Zhu Yuanyuan Zhang Bo Liu |
author_sort | Xiaodi Xu |
collection | DOAJ |
description | The most economically important trait of the <i>Procambarus clarkii</i> is meat quality. Protein deposition is essential in muscle growth and nutritional quality formation. The effects and potential mechanisms of feed protein sources on crustaceans’ muscle protein deposition have not been elucidated. This study established an all-animal protein source (AP) and an all-plant protein source group (PP), with a feeding period of 8 weeks (four replicates per group, 45 individuals per replicate). The results demonstrated that muscle protein deposition, muscle fiber diameter, and hardness were significantly higher in the PP group (<i>p</i> < 0.05). The transcript levels of genes involved in protein synthesis were notably upregulated, while those of protein hydrolysis and negative regulators of myogenesis notably downregulated in PP group (<i>p</i> < 0.05). Furthermore, protein sources shaped differential intestinal microbiota composition and microbial metabolites profiles, as evidenced by a significant decrease in g_<i>Bacteroides</i> (<i>p</i> = 0.030), and a significant increase in taurochenodeoxycholic acid (TCDCA) in PP group (<i>p</i> = 0.027). A significant correlation was further established by Pearson correlation analysis between the g_<i>Bacteroides</i>, TCDCA, and genes involved in the <i>MSTN</i>-mediated protein deposition pathway (<i>p</i> < 0.05). In vitro anaerobic fermentation confirmed the ability of the two groups of intestinal flora to metabolically produce differential TCDCA (<i>p</i> = 0.038). Our results demonstrated that the ‘<i>Bacteroides</i>-TCDCA-<i>MSTN</i>’ axis may mediate the effects of different protein sources on muscle development and protein deposition in <i>P. clarkii</i>, which was anticipated to represent a novel target for the muscle quality modulation in crustaceans. |
format | Article |
id | doaj-art-16b374f5b5374a47bc946cf71f7f923d |
institution | Kabale University |
issn | 2076-2607 |
language | English |
publishDate | 2024-12-01 |
publisher | MDPI AG |
record_format | Article |
series | Microorganisms |
spelling | doaj-art-16b374f5b5374a47bc946cf71f7f923d2025-01-24T13:42:17ZengMDPI AGMicroorganisms2076-26072024-12-011311110.3390/microorganisms13010011The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i>Xiaodi Xu0Xiaochuan Zheng1Qunlan Zhou2Cunxin Sun3Aimin Wang4Aimin Zhu5Yuanyuan Zhang6Bo Liu7Wuxi Fisheries College, Nanjing Agricultural University, Wuxi 214128, ChinaWuxi Fisheries College, Nanjing Agricultural University, Wuxi 214128, ChinaWuxi Fisheries College, Nanjing Agricultural University, Wuxi 214128, ChinaWuxi Fisheries College, Nanjing Agricultural University, Wuxi 214128, ChinaCollege of Marine and Biology Engineering, Yancheng Institute of Technology, Yancheng 224051, ChinaYancheng Academy of Fishery Science, Yancheng 224051, ChinaShandong Freshwater Fisheries Research Institute, Jinan 250013, ChinaWuxi Fisheries College, Nanjing Agricultural University, Wuxi 214128, ChinaThe most economically important trait of the <i>Procambarus clarkii</i> is meat quality. Protein deposition is essential in muscle growth and nutritional quality formation. The effects and potential mechanisms of feed protein sources on crustaceans’ muscle protein deposition have not been elucidated. This study established an all-animal protein source (AP) and an all-plant protein source group (PP), with a feeding period of 8 weeks (four replicates per group, 45 individuals per replicate). The results demonstrated that muscle protein deposition, muscle fiber diameter, and hardness were significantly higher in the PP group (<i>p</i> < 0.05). The transcript levels of genes involved in protein synthesis were notably upregulated, while those of protein hydrolysis and negative regulators of myogenesis notably downregulated in PP group (<i>p</i> < 0.05). Furthermore, protein sources shaped differential intestinal microbiota composition and microbial metabolites profiles, as evidenced by a significant decrease in g_<i>Bacteroides</i> (<i>p</i> = 0.030), and a significant increase in taurochenodeoxycholic acid (TCDCA) in PP group (<i>p</i> = 0.027). A significant correlation was further established by Pearson correlation analysis between the g_<i>Bacteroides</i>, TCDCA, and genes involved in the <i>MSTN</i>-mediated protein deposition pathway (<i>p</i> < 0.05). In vitro anaerobic fermentation confirmed the ability of the two groups of intestinal flora to metabolically produce differential TCDCA (<i>p</i> = 0.038). Our results demonstrated that the ‘<i>Bacteroides</i>-TCDCA-<i>MSTN</i>’ axis may mediate the effects of different protein sources on muscle development and protein deposition in <i>P. clarkii</i>, which was anticipated to represent a novel target for the muscle quality modulation in crustaceans.https://www.mdpi.com/2076-2607/13/1/11<i>Procambarus clarkii</i>protein sourceprotein depositiontaurochenodeoxycholic acidintestinal microbiota |
spellingShingle | Xiaodi Xu Xiaochuan Zheng Qunlan Zhou Cunxin Sun Aimin Wang Aimin Zhu Yuanyuan Zhang Bo Liu The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> Microorganisms <i>Procambarus clarkii</i> protein source protein deposition taurochenodeoxycholic acid intestinal microbiota |
title | The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> |
title_full | The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> |
title_fullStr | The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> |
title_full_unstemmed | The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> |
title_short | The Bile Acid Metabolism of Intestinal Microorganisms Mediates the Effect of Different Protein Sources on Muscle Protein Deposition in <i>Procambarus clarkii</i> |
title_sort | bile acid metabolism of intestinal microorganisms mediates the effect of different protein sources on muscle protein deposition in i procambarus clarkii i |
topic | <i>Procambarus clarkii</i> protein source protein deposition taurochenodeoxycholic acid intestinal microbiota |
url | https://www.mdpi.com/2076-2607/13/1/11 |
work_keys_str_mv | AT xiaodixu thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT xiaochuanzheng thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT qunlanzhou thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT cunxinsun thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT aiminwang thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT aiminzhu thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT yuanyuanzhang thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT boliu thebileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT xiaodixu bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT xiaochuanzheng bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT qunlanzhou bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT cunxinsun bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT aiminwang bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT aiminzhu bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT yuanyuanzhang bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii AT boliu bileacidmetabolismofintestinalmicroorganismsmediatestheeffectofdifferentproteinsourcesonmuscleproteindepositioniniprocambarusclarkiii |