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...

Full description

Saved in:
Bibliographic Details
Main Authors: Xiaodi Xu, Xiaochuan Zheng, Qunlan Zhou, Cunxin Sun, Aimin Wang, Aimin Zhu, Yuanyuan Zhang, Bo Liu
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