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Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish

BACKGROUND: The development of a sustainable business model with social acceptance, makes necessary to develop new strategies to guarantee the growth, health, and well-being of farmed animals. Debaryomyces hansenii is a yeast species that can be used as a probiotic in aquaculture due to its capacity...

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Autores principales: Sanahuja, Ignasi, Ruiz, Alberto, Firmino, Joana P., Reyes-López, Felipe E., Ortiz-Delgado, Juan B., Vallejos-Vidal, Eva, Tort, Lluis, Tovar-Ramírez, Dariel, Cerezo, Isabel M., Moriñigo, Miguel A., Sarasquete, Carmen, Gisbert, Enric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10329801/
https://www.ncbi.nlm.nih.gov/pubmed/37422657
http://dx.doi.org/10.1186/s40104-023-00895-4
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author Sanahuja, Ignasi
Ruiz, Alberto
Firmino, Joana P.
Reyes-López, Felipe E.
Ortiz-Delgado, Juan B.
Vallejos-Vidal, Eva
Tort, Lluis
Tovar-Ramírez, Dariel
Cerezo, Isabel M.
Moriñigo, Miguel A.
Sarasquete, Carmen
Gisbert, Enric
author_facet Sanahuja, Ignasi
Ruiz, Alberto
Firmino, Joana P.
Reyes-López, Felipe E.
Ortiz-Delgado, Juan B.
Vallejos-Vidal, Eva
Tort, Lluis
Tovar-Ramírez, Dariel
Cerezo, Isabel M.
Moriñigo, Miguel A.
Sarasquete, Carmen
Gisbert, Enric
author_sort Sanahuja, Ignasi
collection PubMed
description BACKGROUND: The development of a sustainable business model with social acceptance, makes necessary to develop new strategies to guarantee the growth, health, and well-being of farmed animals. Debaryomyces hansenii is a yeast species that can be used as a probiotic in aquaculture due to its capacity to i) promote cell proliferation and differentiation, ii) have immunostimulatory effects, iii) modulate gut microbiota, and/or iv) enhance the digestive function. To provide inside into the effects of D. hansenii on juveniles of gilthead seabream (Sparus aurata) condition, we integrated the evaluation of the main key performance indicators coupled with the integrative analysis of the intestine condition, through histological and microbiota state, and its transcriptomic profiling. RESULTS: After 70 days of a nutritional trial in which a diet with low levels of fishmeal (7%) was supplemented with 1.1% of D. hansenii (17.2 × 10(5) CFU), an increase of ca. 12% in somatic growth was observed together with an improvement in feed conversion in fish fed a yeast-supplemented diet. In terms of intestinal condition, this probiotic modulated gut microbiota without affecting the intestine cell organization, whereas an increase in the staining intensity of mucins rich in carboxylated and weakly sulphated glycoconjugates coupled with changes in the affinity for certain lectins were noted in goblet cells. Changes in microbiota were characterized by the reduction in abundance of several groups of Proteobacteria, especially those characterized as opportunistic groups. The microarrays-based transcriptomic analysis found 232 differential expressed genes in the anterior-mid intestine of S. aurata, that were mostly related to metabolic, antioxidant, immune, and symbiotic processes. CONCLUSIONS: Dietary administration of D. hansenii enhanced somatic growth and improved feed efficiency parameters, results that were coupled to an improvement of intestinal condition as histochemical and transcriptomic tools indicated. This probiotic yeast stimulated host-microbiota interactions without altering the intestinal cell organization nor generating dysbiosis, which demonstrated its safety as a feed additive. At the transcriptomic level, D. hansenii promoted metabolic pathways, mainly protein-related, sphingolipid, and thymidylate pathways, in addition to enhance antioxidant-related intestinal mechanisms, and to regulate sentinel immune processes, potentiating the defensive capacity meanwhile maintaining the homeostatic status of the intestine. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-023-00895-4.
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spelling pubmed-103298012023-07-10 Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish Sanahuja, Ignasi Ruiz, Alberto Firmino, Joana P. Reyes-López, Felipe E. Ortiz-Delgado, Juan B. Vallejos-Vidal, Eva Tort, Lluis Tovar-Ramírez, Dariel Cerezo, Isabel M. Moriñigo, Miguel A. Sarasquete, Carmen Gisbert, Enric J Anim Sci Biotechnol Research BACKGROUND: The development of a sustainable business model with social acceptance, makes necessary to develop new strategies to guarantee the growth, health, and well-being of farmed animals. Debaryomyces hansenii is a yeast species that can be used as a probiotic in aquaculture due to its capacity to i) promote cell proliferation and differentiation, ii) have immunostimulatory effects, iii) modulate gut microbiota, and/or iv) enhance the digestive function. To provide inside into the effects of D. hansenii on juveniles of gilthead seabream (Sparus aurata) condition, we integrated the evaluation of the main key performance indicators coupled with the integrative analysis of the intestine condition, through histological and microbiota state, and its transcriptomic profiling. RESULTS: After 70 days of a nutritional trial in which a diet with low levels of fishmeal (7%) was supplemented with 1.1% of D. hansenii (17.2 × 10(5) CFU), an increase of ca. 12% in somatic growth was observed together with an improvement in feed conversion in fish fed a yeast-supplemented diet. In terms of intestinal condition, this probiotic modulated gut microbiota without affecting the intestine cell organization, whereas an increase in the staining intensity of mucins rich in carboxylated and weakly sulphated glycoconjugates coupled with changes in the affinity for certain lectins were noted in goblet cells. Changes in microbiota were characterized by the reduction in abundance of several groups of Proteobacteria, especially those characterized as opportunistic groups. The microarrays-based transcriptomic analysis found 232 differential expressed genes in the anterior-mid intestine of S. aurata, that were mostly related to metabolic, antioxidant, immune, and symbiotic processes. CONCLUSIONS: Dietary administration of D. hansenii enhanced somatic growth and improved feed efficiency parameters, results that were coupled to an improvement of intestinal condition as histochemical and transcriptomic tools indicated. This probiotic yeast stimulated host-microbiota interactions without altering the intestinal cell organization nor generating dysbiosis, which demonstrated its safety as a feed additive. At the transcriptomic level, D. hansenii promoted metabolic pathways, mainly protein-related, sphingolipid, and thymidylate pathways, in addition to enhance antioxidant-related intestinal mechanisms, and to regulate sentinel immune processes, potentiating the defensive capacity meanwhile maintaining the homeostatic status of the intestine. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-023-00895-4. BioMed Central 2023-07-09 /pmc/articles/PMC10329801/ /pubmed/37422657 http://dx.doi.org/10.1186/s40104-023-00895-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Sanahuja, Ignasi
Ruiz, Alberto
Firmino, Joana P.
Reyes-López, Felipe E.
Ortiz-Delgado, Juan B.
Vallejos-Vidal, Eva
Tort, Lluis
Tovar-Ramírez, Dariel
Cerezo, Isabel M.
Moriñigo, Miguel A.
Sarasquete, Carmen
Gisbert, Enric
Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title_full Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title_fullStr Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title_full_unstemmed Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title_short Debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
title_sort debaryomyces hansenii supplementation in low fish meal diets promotes growth, modulates microbiota and enhances intestinal condition in juvenile marine fish
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10329801/
https://www.ncbi.nlm.nih.gov/pubmed/37422657
http://dx.doi.org/10.1186/s40104-023-00895-4
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