# Effect of Quinoa Germ Meal as a Replacement for Fish Meal in Diets on Intestinal Health of Juvenile Turbot (Scophthalmus maximus)

**Authors:** Jingkun Yang, Zhibin Sun, Cong Ma, Xinan Wang, Zhifeng Liu, Zhihui Huang, Yunyi Gao, Yuanyuan Li, Yilin Wang, Aijun Ma

PMC · DOI: 10.3390/biology15040304 · Biology · 2026-02-09

## TL;DR

This study explores using quinoa germ meal as a fish meal replacement in turbot diets, finding that high levels negatively affect growth and intestinal health.

## Contribution

The study provides new insights into the effects of quinoa germ meal on intestinal health and gene expression in juvenile turbot.

## Key findings

- High quinoa germ meal inclusion levels impaired growth performance in juvenile turbot.
- Transcriptomic analysis showed modulation of ribosome-related and protein digestion pathways.
- Low quinoa germ meal levels (≤20%) had minimal adverse effects on turbot health.

## Abstract

This study investigates the potential of quinoa germ meal as a dietary alternative protein source for juvenile turbot. Five experimental diets were formulated, comprising a control group and four experimental groups with replacement levels of 10%, 20%, 30%, and 40%. With increasing replacement levels, most growth parameters, notably feed intake, declined significantly. All experimental groups displayed decreased muscle crude lipid content and altered intestinal morphology. Transcriptome analysis revealed that quinoa germ meal modulated gene expression in ribosome-related and protein digestion and absorption pathways, and notably, high replacement levels activated the cellular senescence pathway in the intestine. These findings provide a theoretical basis for optimizing quinoa germ meal as a sustainable protein source in aquaculture.

Quinoa germ meal (QGM) is a protein-rich by-product with potential as an alternative protein source; however, its effects on growth performance and intestinal health in marine carnivorous fish remain unclear. Juvenile turbot (Scophthalmus maximus) were fed five isonitrogenous (45.6% crude protein) and isolipidic (9.8% crude lipid) diets for 8 weeks: a fishmeal-based control diet (C) and four experimental diets in which fishmeal was replaced with QGM at 10% (Q10), 20% (Q20), 30% (Q30), and 40% (Q40). Growth performance, muscle proximate composition, intestinal histomorphology, and intestinal transcriptomic profiles were analyzed. Growth performance parameters, including final body weight, weight gain rate, specific growth rate, daily feed intake, and condition factor, decreased significantly with increasing QGM inclusion levels compared with the control (p < 0.05). Feed conversion ratio increased significantly only when replacement exceeded 30% (p < 0.05), while survival rate was unaffected (p > 0.05). Muscle crude lipid content was significantly reduced in all QGM-fed groups (p < 0.05), whereas crude protein, moisture, and ash contents were unchanged. Intestinal mucosal fold height increased in the Q30 and Q40 groups, while submucosal width decreased in the Q40 group (p < 0.05). Transcriptomic analysis revealed a dose-dependent increase in differentially expressed genes, mainly enriched in ribosome-related pathways, linoleic acid metabolism, and protein digestion and absorption. High dietary inclusion of QGM (>30%) impaired growth performance in juvenile turbot, whereas low inclusion levels (≤20%) exerted minimal adverse effects. Quinoa germ meal represents a potential alternative protein source, yet its effective utilization requires further optimization to maintain growth performance.

## Linked entities

- **Species:** Scophthalmus maximus (taxon 52904)

## Full-text entities

- **Genes:** MYC (MYC proto-oncogene, bHLH transcription factor) [NCBI Gene 4609] {aka MRTL, MYCC, bHLHe39, c-Myc}, RHEB (Ras homolog, mTORC1 binding) [NCBI Gene 6009] {aka RHEB2}, CDK2 (cyclin dependent kinase 2) [NCBI Gene 1017] {aka CDKN2, p33(CDK2)}, FOXM1 (forkhead box M1) [NCBI Gene 2305] {aka FKHL16, FOXM1A, FOXM1B, FOXM1C, HFH-11, HFH11}, CAPN1 (calpain 1) [NCBI Gene 823] {aka CANP, CANP1, CANPL1, SPG76, muCANP, muCL}, MYBL2 (MYB proto-oncogene like 2) [NCBI Gene 4605] {aka B-MYB, BMYB}, CCNE1 (cyclin E1) [NCBI Gene 898] {aka CCNE, pCCNE1}, CCNA2 (cyclin A2) [NCBI Gene 890] {aka CCN1, CCNA}, TP53 (tumor protein p53) [NCBI Gene 7157] {aka BCC7, BMFS5, LFS1, P53, TRP53}, CDKN1A (cyclin dependent kinase inhibitor 1A) [NCBI Gene 1026] {aka CAP20, CDKN1, CIP1, MDA-6, P21, SDI1}, EIF4EBP1 (eukaryotic translation initiation factor 4E binding protein 1) [NCBI Gene 1978] {aka 4E-BP1, 4EBP1, BP-1, PHAS-I}, MHC class I antigen [NCBI Gene 100507703], E2F2 (E2F transcription factor 2) [NCBI Gene 1870] {aka E2F-2}, MTOR (mechanistic target of rapamycin kinase) [NCBI Gene 2475] {aka FRAP, FRAP1, FRAP2, RAFT1, RAPT1, SKS}, TGFB1 (transforming growth factor beta 1) [NCBI Gene 7040] {aka CAEND1, CED, DPD1, IBDIMDE, LAP, TGF-beta1}, HIPK2 (homeodomain interacting protein kinase 2) [NCBI Gene 28996] {aka PRO0593}, HLA-G (major histocompatibility complex, class I, G) [NCBI Gene 3135] {aka MHC-G}, NFATC1 (nuclear factor of activated T cells 1) [NCBI Gene 4772] {aka NF-ATC, NF-ATc1.2, NFAT2, NFATc}, SERPINE1 (serpin family E member 1) [NCBI Gene 5054] {aka PAI, PAI-1, PAI1, PLANH1}
- **Diseases:** inflammatory (MESH:D007249), injury to (MESH:D014947), CF (MESH:D003550), weight gain (MESH:D015430), QGM (MESH:D009373), nutrient deficiency (MESH:D007153), SASP (MESH:D008579), enteritis (MESH:D004751), intestinal dilation (MESH:D007410)
- **Chemicals:** sodium chloride (MESH:D012965), Vitamin K3 (MESH:D024483), proline (MESH:D011392), linoleic acid (MESH:D019787), Vitamin A acetate (MESH:C009166), paraffin (MESH:D010232), methionine (MESH:D008715), pyridoxine hydrochloride (MESH:D011736), nitrogen (MESH:D009584), Vitamin E (MESH:D014810), histidine (MESH:D006639), xylene (MESH:D014992), Alanine (MESH:D000409), ferrous sulfate (MESH:C020748), triglycerides (MESH:D014280), valine (MESH:D014633), alpha-linolenic acid (MESH:D017962), niacinamide (MESH:D009536), tyrosine (MESH:D014443), phospholipid (MESH:D010743), leucine (MESH:D007930), amide (MESH:D000577), Vitamin A (MESH:D014801), TRIzol (MESH:C411644), nucleotide (MESH:D009711), arachidonic acid (MESH:D016718), acetyl-CoA (MESH:D000105), peptide (MESH:D010455), glutamate (MESH:D018698), Vitamin C (MESH:D001205), copper (MESH:D003300), fish oil (MESH:D005395), essential amino acid (MESH:D000601), biotin (MESH:D001710), pyrimidine (MESH:C030986), glycine (MESH:D005998), cholesterol (MESH:D002784), ethanol (MESH:D000431), H&amp;E (MESH:D006371), QGM (-), hematoxylin (MESH:D006416), copper sulfate (MESH:D019327), cystine (MESH:D003553), zeolite (MESH:D017641), Amino Acid (MESH:D000596), magnesium sulfate (MESH:D008278), Vitamin D3 (MESH:D002762), Vitamin B1 (MESH:D013831), aspartate (MESH:D001224), sodium selenite (MESH:D018038), carbohydrate (MESH:D002241), fatty acid (MESH:D005227), arginine (MESH:D001120), cholesteryl ester (MESH:D002788), starch (MESH:D013213), Vitamin B2 (MESH:D012256), Phenylalanine (MESH:D010649), serine (MESH:D012694), beta-alanine (MESH:D015091), glutathione (MESH:D005978)
- **Species:** Glycine max (soybean, species) [taxon 3847], Escherichia coli (E. coli, species) [taxon 562], Scophthalmus maximus (turbot, species) [taxon 52904], Chenopodium quinoa (quinoa, species) [taxon 63459], Fenestella gardiennetii (species) [taxon 2499855], Oreochromis niloticus (Nile tilapia, species) [taxon 8128], Powellomyces sp. EA (species) [taxon 252690], Danio rerio (leopard danio, species) [taxon 7955], Oncorhynchus mykiss (rainbow trout, species) [taxon 8022], Homo sapiens (human, species) [taxon 9606], Salmo salar (Atlantic salmon, species) [taxon 8030], Pangasianodon hypophthalmus (iridescent shark-catfish, species) [taxon 310915]

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## Figures

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## References

76 references — full list in the complete paper: https://tomesphere.com/paper/PMC12938430/full.md

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Source: https://tomesphere.com/paper/PMC12938430