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Physiological and transcriptomic effects of formulated diets including the prebiotics inulin, β-glucan, and chitosan on juveniles of Totoaba macdonaldi

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Abstract

In this study, we evaluated the effects of three prebiotics (inulin, β-glucan, and chitosan) on the physiological performance of Totoaba macdonaldi juveniles under culture conditions. The respiratory burst and the leucocyte content were measured in the blood to assess innate immune responses. The intestinal digestive capacity was evaluated by analyzing trypsin, amylase, and lipase activities, whereas the effects of such prebiotics at the transcriptomic level were assessed by implementing the RNA-Seq of liver tissue. After 60 days, fish fed with 0.5% chitosan diets showed the highest respiratory burst, the lowest lipase activity, and the highest number of differentially expressed genes (DEGs), where biological processes related to proteolysis, digestion, and lipid hydroxylation were the most affected. In addition, fish from the chitosan diet showed the highest expression of immunoglobulin genes. In contrast, fish fed with the 1% inulin diet presented the highest diet digestibility and trypsin and lipase activities. These physiological effects align with the highest expression of trypsin-like and chymotrypsin-like genes in the liver of fish from this diet. On the other hand, fish fed the 0.1% β-glucan diets showed the lowest amount of DEGs compared to the control group, most of which were associated with immune response, with an up-regulation of genes related to the complement system and a downregulation of immunoglobulin genes. Based on our results, we propose the inclusion of 1% dietary inulin to improve the digestibility of experimental diets and the addition of 0.5% chitosan to stimulate the immune system of T. macdonaldi juveniles.

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Funding

This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT, México) through the Centro de Investigación Científica y Educación Superior de Ensenada, Baja California (CICESE) internal projects (grant number 623112 to JPL, 623159 to FLDC, and 682136 to CEGS). Additional funding was provided by the Agencia Nacional de Investigación y Desarrollo (ANID) Proyecto PAI Inserción en la Academia (grant number PAI79170033), Proyecto Fondecyt de Iniciación (grant number 11180084) and Proyecto Fondecyt Regular (grant number 1220708) to FA. The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

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Authors and Affiliations

Authors

Contributions

JPL: conceptualization; funding acquisition; investigation; methodology; project administration; resources; supervision; writing—review and editing.

OEJ: data curation, formal analysis; visualization; writing—original draft; writing—review and editing.

FLDC: conceptualization; funding acquisition; resources; methodology; writing—review and editing.

SE: data curation; formal analysis; investigation; writing—original draft.

ELL: data curation; investigation; writing—review and editing.

CM: data curation; formal analysis; visualization.

FA: data curation; formal analysis; funding acquisition; visualization; writing—review and editing.

CEGS: conceptualization; funding acquisition; methodology; resources; writing—review and editing.

Corresponding authors

Correspondence to Fabiola Lafarga-De la Cruz or Juan Pablo Lazo.

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Ethical approval

This research meets the ARRIVE, European Union Council (2010/63/EU), and Mexican Government (NOM-062—ZOO-1999) guidelines for the production, care, and use of experimental animals. Fish were humanely euthanized according to CICESE’s fish culture animal-care standards and protocols (Juárez et al. 2021).

Competing interests

The authors declare no competing interests.

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Handling editor: Daniel Merrifield

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Highlights

•Each prebiotic diet caused a unique physiological response in juvenile totoaba.

•The inclusion of inulin (1%) improved the digestibility of the experimental diet.

•The β-glucan diet (0.1%) upregulated genes of the complement system in the liver.

•The chitosan diet (0.5%) stimulated innate and adaptive immune responses.

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Juárez, O.E., Galindo-Sánchez, C.E., la Cruz, F.LD. et al. Physiological and transcriptomic effects of formulated diets including the prebiotics inulin, β-glucan, and chitosan on juveniles of Totoaba macdonaldi. Aquacult Int 32, 61–85 (2024). https://doi.org/10.1007/s10499-023-01144-1

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