Metabonomic and microbiomic analysis reveals the effect of sargassum enzyme hydrolysate compound fish protein hydrolysate on the intestinal health in Pacific white shrimp (Penaeus vannamei)
Yi Luo, Jinqi Xu, Songming Chen, Qiang Chen, Runzhe Zhang, Jiangyang Yin, Tao Han, Jiteng Wang
{"title":"Metabonomic and microbiomic analysis reveals the effect of sargassum enzyme hydrolysate compound fish protein hydrolysate on the intestinal health in Pacific white shrimp (Penaeus vannamei)","authors":"Yi Luo, Jinqi Xu, Songming Chen, Qiang Chen, Runzhe Zhang, Jiangyang Yin, Tao Han, Jiteng Wang","doi":"10.1016/j.cbd.2025.101568","DOIUrl":null,"url":null,"abstract":"<div><div>The investigation of geographical feed raw materials is crucial to maintain the sustainable development of aquaculture. Ensuring the intestinal health of aquatic animals is the key to improving the absorption and utilization rate of new protein sources. In the present study, a composite protein source derived from the sargassum enzyme-hydrolysate compound fish protein hydrolysate (“SFPH” in the experiment) was utilized to replace 0 %, 5 %, 10 %, 20 %, 30 %, and 40 % of fish meal protein, respectively. Pacific white shrimp (<em>Penaeus vannamei</em>) with an initial weight of 0.9 g was used as experimental model for an 8-week feeding trial. The results revealed that SFPH replacement reduced the width of intestinal microvilli, but the 5%SFPH group significantly increased intestinal wall thickness and microvilli height. Antioxidant indicators analysis revealed that when over 10 % of fish meal protein was substituted with SFPH, the total antioxidant capacity dramatically decreased. When SFPH replaced 40 % of fish meal protein, the mRNA expression levels of endoplasmic reticulum stress-related indicators (<em>bip</em> and <em>atf4</em>) significantly increased, as well as the genes associated with apoptosis (<em>jnk</em>, <em>caspase 8</em> and <em>caspase 3</em>). The analysis of intestinal microbiota showed that the 5%SFPH group significantly increased the richness of intestinal microbiota and significantly increased the abundance of beneficial bacteria (<em>Campilobacter</em>, <em>Patescibacter</em>, <em>Deferribacter</em> and <em>Halobacter</em>). The 40%SFPH group significantly increased the abundance of pathogenic bacteria (<em>Pseudomonas</em>, <em>Serratia</em>, <em>Rickettsia, Edwardsiella</em>, and <em>Veillonella</em>). A total of 201 differential relative abundance metabolites were detected by metabolomics, among which the contents of succinate, oxidized glutathione and reduced glutathione were reduced in the 40%SFPH group. The differential metabolites were mainly enriched in cysteine and methionine metabolism, biosynthesis of amino acid and glutathione metabolism. Based on the integrated analysis of metabolomics and intestinal microbiota, changes in signal pathways such as amino acid metabolism and glutathione synthesis may be the main reasons for the high proportion of SFPH disrupting intestinal health. This study provides in-depth data on the reaction mechanisms of shrimp to seaweed protein, and also provides new directions for the improvement of seaweed protein in the future.</div></div>","PeriodicalId":55235,"journal":{"name":"Comparative Biochemistry and Physiology D-Genomics & Proteomics","volume":"56 ","pages":"Article 101568"},"PeriodicalIF":2.2000,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Comparative Biochemistry and Physiology D-Genomics & Proteomics","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1744117X25001571","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The investigation of geographical feed raw materials is crucial to maintain the sustainable development of aquaculture. Ensuring the intestinal health of aquatic animals is the key to improving the absorption and utilization rate of new protein sources. In the present study, a composite protein source derived from the sargassum enzyme-hydrolysate compound fish protein hydrolysate (“SFPH” in the experiment) was utilized to replace 0 %, 5 %, 10 %, 20 %, 30 %, and 40 % of fish meal protein, respectively. Pacific white shrimp (Penaeus vannamei) with an initial weight of 0.9 g was used as experimental model for an 8-week feeding trial. The results revealed that SFPH replacement reduced the width of intestinal microvilli, but the 5%SFPH group significantly increased intestinal wall thickness and microvilli height. Antioxidant indicators analysis revealed that when over 10 % of fish meal protein was substituted with SFPH, the total antioxidant capacity dramatically decreased. When SFPH replaced 40 % of fish meal protein, the mRNA expression levels of endoplasmic reticulum stress-related indicators (bip and atf4) significantly increased, as well as the genes associated with apoptosis (jnk, caspase 8 and caspase 3). The analysis of intestinal microbiota showed that the 5%SFPH group significantly increased the richness of intestinal microbiota and significantly increased the abundance of beneficial bacteria (Campilobacter, Patescibacter, Deferribacter and Halobacter). The 40%SFPH group significantly increased the abundance of pathogenic bacteria (Pseudomonas, Serratia, Rickettsia, Edwardsiella, and Veillonella). A total of 201 differential relative abundance metabolites were detected by metabolomics, among which the contents of succinate, oxidized glutathione and reduced glutathione were reduced in the 40%SFPH group. The differential metabolites were mainly enriched in cysteine and methionine metabolism, biosynthesis of amino acid and glutathione metabolism. Based on the integrated analysis of metabolomics and intestinal microbiota, changes in signal pathways such as amino acid metabolism and glutathione synthesis may be the main reasons for the high proportion of SFPH disrupting intestinal health. This study provides in-depth data on the reaction mechanisms of shrimp to seaweed protein, and also provides new directions for the improvement of seaweed protein in the future.
期刊介绍:
Comparative Biochemistry & Physiology (CBP) publishes papers in comparative, environmental and evolutionary physiology.
Part D: Genomics and Proteomics (CBPD), focuses on “omics” approaches to physiology, including comparative and functional genomics, metagenomics, transcriptomics, proteomics, metabolomics, and lipidomics. Most studies employ “omics” and/or system biology to test specific hypotheses about molecular and biochemical mechanisms underlying physiological responses to the environment. We encourage papers that address fundamental questions in comparative physiology and biochemistry rather than studies with a focus that is purely technical, methodological or descriptive in nature.