SEARCHCROSS-SECTIONALaquaculture, veterinary_science

cross-sectional·aquaculture, veterinary_science, microbiology, metabolomics·PMC10177557

Alterations of the Gut Microbiota and Metabolomics Associated with the Different Growth Performances of Macrobrachium rosenbergii Families

Animals : an Open Access Journal from MDPI · 8 authors, 2 centres

AI SUMMARY

FIDELITY 100%

POPULATION90 families of Macrobrachium rosenbergii (giant freshwater prawn), 150 juveniles per family, initial body weight 2.39 ± 0.29 g

INTERVENTIONNot applicable — observational study comparing families with naturally differing growth performance under identical feeding conditions

COMPARISONHigh (H), medium (M), and low (L) growth performance groups based on weight gain and specific growth rate after 92 days of culture

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TL;DR

This study investigated gut microbiota and intestinal metabolites in 90 families of giant freshwater prawns (Macrobrachium rosenbergii) with different growth rates using 16S rRNA sequencing and LC–MS metabolomics. Fast-growing prawns had higher abundances of beneficial bacteria like Lactobacillus and Blautia, along with elevated levels of metabolites involved in arginine, taurine, and fatty acid metabolism. These findings suggest that specific gut microbes and their metabolic products may serve as biomarkers for selective breeding and probiotic feed development in prawn aquaculture.

Full summary

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**Background:** The giant freshwater prawn (GFP; Macrobrachium rosenbergii) is an economically important aquaculture species, but genetically improved varieties are needed to meet growing demand. The gut microbiota plays critical roles in nutrient absorption, metabolism, immunity, and growth in aquatic animals. However, the specific gut microbiota and metabolites associated with growth performance in GFP families had not been characterized. This study aimed to identify key intestinal bacteria and metabolites linked to different growth performances in GFP families using 16S rRNA sequencing and LC–MS metabolomics.

**Methods:** A total of 90 GFP families were bred and cultured separately in cement tanks (15 m² each) under identical conditions for 92 days. Water temperature was maintained at 28 ± 2 °C, pH 7.5–8, dissolved oxygen ≥ 5.5 mg/L, ammonia nitrogen ≤ 0.25 mg/L, and nitrite ≤ 0.1 mg/L. Prawns were fed a formula diet (crude protein ≥ 38%, crude fat ≥ 5%) twice daily. After 92 days, families were divided into high (H), medium (M), and low (L) growth performance groups based on weight gain (WG) and specific growth rate (SGR). Three families per group were randomly selected. Intestinal samples from 28 individuals per family were collected under sterile conditions. DNA was extracted using the CTAB method, and the V3-V4 region of the 16S rRNA gene was amplified and sequenced on an Illumina NovaSeq 6000 platform. Metabolites were extracted from intestinal tissues and analyzed using Waters 2D UPLC tandem Q Exactive high-resolution mass spectrometry. Differential metabolites were identified using VIP ≥ 1, FC ≥ 1.2 or ≤ 0.83, and q < 0.05. Pearson correlation and Mantel test were used for microbiota–metabolite correlation analysis.

**Key Results:** Group H had significantly higher (p < 0.001) final body weight (41.03 ± 1.44 g), weight gain (1616.82 ± 60.08%), and SGR (3.09 ± 0.04 %/d) compared to Group M (37.46 ± 0.73 g, 1467.45 ± 30.54%, 2.99 ± 0.02 %/d) and Group L (33.34 ± 1.97 g, 1294.82 ± 82.31%, 2.86 ± 0.07 %/d). Group H had the highest OTU richness (1800 OTUs) versus Group M (1461) and Group L (796). The relative abundance of Firmicutes was 14.2% in Group H, 9.7% in Group M, and 4.4% in Group L, while Proteobacteria was 83.7%, 88.3%, and 92.8%, respectively. Key bacteria enriched in Group H included Lactobacillus (0.431% vs. 0.007% in M and 0.001% in L), Blautia (0.043% vs. 0.003% and 0.0005%), Lachnospiraceae (0.502% vs. 0.027% and 0.007%), and Romboutsia (0.111% vs. 0.003% and 0.001%). Metabolomic analysis identified 1173 significantly different metabolites in ESI+ mode and 428 in ESI− mode. Spermidine levels were 7,568,085.52 in Group H vs. 503,668.63 in M and 297,921.56 in L. Adenosine was 20,948,251.26 in H vs. 16,955,727.72 in M and 5,034,361.71 in L. L-citrulline was lower in H (12,351,334.96) than in M (28,501,478.19) and L (50,349,665.38). Correlation analysis showed that Lactobacillus and Blautia abundances were positively correlated with alpha-ketoglutaric acid and L-arginine levels. Blautia was also positively correlated with adenosine, taurine, and spermidine. KEGG enrichment revealed that pathways related to arginine and proline metabolism, arginine biosynthesis, taurine and hypotaurine metabolism, arachidonic acid metabolism, and alpha-linolenic acid metabolism were significantly enriched in Group H.

**Clinical Implications:** This study provides the first comprehensive characterization of gut microbiota and intestinal metabolites associated with growth performance in M. rosenbergii families. The identification of specific bacterial genera (Lactobacillus, Blautia, Faecalibacterium, Butyricicoccus) and metabolites (spermidine, adenosine, arginine-related compounds, unsaturated fatty acids) that are enriched in fast-growing prawns offers potential biomarkers for selective breeding programs. The findings also support the development of probiotic feeds targeting these beneficial microbes to enhance growth performance in aquaculture. The integration of 16S rRNA sequencing with metabolomics provides a framework for understanding host–microbe interactions in crustacean growth regulation.

PICO

PPOPULATION

90 families of Macrobrachium rosenbergii (giant freshwater prawn), 150 juveniles per family, initial body weight 2.39 ± 0.29 g

IINTERVENTION

Not applicable — observational study comparing families with naturally differing growth performance under identical feeding conditions

OOUTCOME

Gut microbiota composition (16S rRNA), intestinal metabolite profiles (LC–MS), and correlations between microbiota and metabolites

STUDY TYPE

cross-sectional

SPECIALTY

aquaculture

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FIDELITY CHECK

100% · A

ORIGINAL PAPER

PMC10177557

Alterations of the Gut Microbiota and Metabolomics Associated with the Different Growth Performances of Macrobrachium rosenbergii Families

Animals : an Open Access Journal from MDPI

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ABSTRACT

Abstract Simple Summary This study used 16S rRNA sequencing and metabolomic methods to investigate the key gut microbiota and metabolites associated with the growth performance of Macrobrachium rosenbergii families. We found that some critical intestinal bacteria, including Lactobacillus and Blautia , and the metabolites related to metabolism of amino acids and fatty acids may play critical roles in the growth of prawns. This study contributes to figuring out the landscape of the gut microflora and intestinal metabolites associated with prawn growth performance and provides a basis for future studies on the probiotic feed of prawns. Abstract To investigate the key gut microbiota and metabolites associated with the growth performance of Macrobrachium rosenbergii families, 16S rRNA sequencing and LC–MS metabolomic methods were used. In this study, 90 M. rosenbergii families were bred to evaluate growth performance. After 92 days of culture, high (H), medium (M), and low (L) experimental groups representing three levels of growth performance, respectively, were collected according to the weight gain and specific growth rate of families. The composition of gut microbiota showed that the relative abundance of Firmicutes, Lachnospiraceae, Lactobacillus, and Blautia were much higher in Group H than those in M and L groups. Meanwhile, compared to the M and L groups, Group H had significantly higher levels of spermidine, adenosine, and creatinine, and lower levels of L-citrulline. Correlation analysis showed that the abundances of Lactobacillus and Blautia were positively correlated with the levels of alpha-ketoglutaric acid and L-arginine. The abundance of Blautia was also positively correlated with the levels of adenosine, taurine, and spermidine. Notably, lots of metabolites related to the metabolism and biosynthesis of arginine, taurine, hypotaurine, and fatty acid were upregulated in Group H. This study contributes to figuring out the landscape of the gut microbiota and metabolites associated with prawn growth performance and provides a basis for selective breeding. Keywords: growth performance, gut bacteria, metabolism, LC–MS

CITATION EXPORT

Xuan Lan, Xin Peng, Tingting Du et al.. Alterations of the Gut Microbiota and Metabolomics Associated with the Different Growth Performances of Macrobrachium rosenbergii Families. Animals : an Open Access Journal from MDPI. (2023). https://doi.org/10.3390/ani13091539

AUTHORS

8 · 2 CENTRES

Xuan Lan, Xin Peng, Tingting Du, Zhenglong Xia, Quanxin Gao, Qiongying Tang, Shaokui Yi, Guoliang Yang

1Zhejiang Provincial Key Laboratory of Aquatic Resources Conservation and Development, Key Laboratory of Aquatic Animal Genetic Breeding and Nutrition, Chinese Academy of Fishery Sciences, College of Life Sciences, Huzhou University, Huzhou 313000, China; [email protected] (X.L.); [email protected] (X.P.); [email protected] (T.D.); [email protected] (Q.G.); [email protected] (Q.T.)
2Jiangsu Shufeng Prawn Breeding Co., Ltd., Gaoyou 225654, China; [email protected]