Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model

The present study explores the effects of two supplementation levels of Debaryomyces hansenii (1.1% and 2.2%) as a probiotic in a reference low fish meal-based diet on the skin mucosal tissue in Sparus aurata. This study includes the evaluation of fish performance coupled with a holistic study of th...

Full description

Bibliographic Details
Main Authors: Ignasi Sanahuja, Laura Fernandez-Alacid, Silvia Torrecillas, Alberto Ruiz, Eva Vallejos-Vidal, Joana P. Firmino, Felipe E. Reyes-Lopez, Lluis Tort, Dariel Tovar-Ramirez, Antoni Ibarz, Enric Gisbert
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1247199/full
_version_ 1797730964264189952
author Ignasi Sanahuja
Laura Fernandez-Alacid
Silvia Torrecillas
Alberto Ruiz
Eva Vallejos-Vidal
Joana P. Firmino
Felipe E. Reyes-Lopez
Lluis Tort
Dariel Tovar-Ramirez
Antoni Ibarz
Enric Gisbert
author_facet Ignasi Sanahuja
Laura Fernandez-Alacid
Silvia Torrecillas
Alberto Ruiz
Eva Vallejos-Vidal
Joana P. Firmino
Felipe E. Reyes-Lopez
Lluis Tort
Dariel Tovar-Ramirez
Antoni Ibarz
Enric Gisbert
author_sort Ignasi Sanahuja
collection DOAJ
description The present study explores the effects of two supplementation levels of Debaryomyces hansenii (1.1% and 2.2%) as a probiotic in a reference low fish meal-based diet on the skin mucosal tissue in Sparus aurata. This study includes the evaluation of fish performance coupled with a holistic study of the skin mucosa: i) a transcriptomic study of the skin tissue, and ii) the evaluation of its secreted mucus both in terms of skin mucosal-associated biomarkers and its defensive capacity by means of co-culture analysis with two pathogenic bacteria. Results showed that after 70 days of diet administration, fish fed the diet supplemented with D. hansenii at 1.1% presented increased somatic growth and a better feed conversion ratio, compared to fish fed the control diet. In contrast, fish fed the diet including 2.2% of the probiotic presented intermediate values. Regarding gene regulation, the probiotic administration at 1.1% resulted in 712 differentially expressed genes (DEGs), among which 53.4% and 46.6% were up- and down-regulated, respectively. In particular, D. hansenii modulated some skin biological processes related to immunity and metabolism. Specifically, D. hansenii administration induced a strong modulation of some immune biological-related processes (61 DEGs), mainly involved in B- and T-cell regulatory pathways. Furthermore, dietary D. hansenii promoted the skin barrier function by the upregulation of anchoring junction genes (23 DEGs), which reinforces the physical defense against potential skin damage. In contrast, the skin showed modulated genes related to extracellular exosome and membrane organization (50 DEGs). This modulated functioning is of great interest, particularly in relation to the increased skin mucus defensive capacity observed in the bacterial co-culture in vitro trials, which could be related to the increased modulation and exudation of the innate immune components from the skin cells into the mucus. In summary, the modulation of innate immune parameters coupled with increased skin barrier function and cell trafficking potentiates the skin’s physical barrier and mucus defensive capacity, while maintaining the skin mucosa’s homeostatic immune and metabolic status. These findings confirmed the advantages of D. hansenii supplementation in low fish meal-based diets, demonstrating the probiotic benefits on cultured marine species.
first_indexed 2024-03-12T11:51:45Z
format Article
id doaj.art-9bd40768382a4b1fbfab9d6f024a6ba7
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-03-12T11:51:45Z
publishDate 2023-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-9bd40768382a4b1fbfab9d6f024a6ba72023-08-31T06:44:24ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-08-011410.3389/fimmu.2023.12471991247199Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish modelIgnasi Sanahuja0Laura Fernandez-Alacid1Silvia Torrecillas2Alberto Ruiz3Eva Vallejos-Vidal4Joana P. Firmino5Felipe E. Reyes-Lopez6Lluis Tort7Dariel Tovar-Ramirez8Antoni Ibarz9Enric Gisbert10Aquaculture Program, Institute of Agrifood Research and Technology (IRTA), La Ràpita, SpainDepartment of Cell Biology, Physiology, and Immunology, University of Barcelona, Barcelona, SpainAquaculture Program, Institute of Agrifood Research and Technology (IRTA), La Ràpita, SpainAquaculture Program, Institute of Agrifood Research and Technology (IRTA), La Ràpita, SpainNúcleo de Investigaciones Aplicadas en Ciencias Veterinarias y Agronómicas, Facultad de Medicina Veterinaria y Agronomía, Universidad de Las Américas, Santiago, ChileAquaculture Program, Institute of Agrifood Research and Technology (IRTA), La Ràpita, SpainCentro de Biotecnología Acuícola, Universidad de Santiago de Chile, Santiago, ChileDepartment of Cell Biology, Physiology, and Immunology, Universitat Autonoma de Barcelona, Barcelona, SpainCentro de Investigaciones Biológicas del Noroeste SC, CIBNOR, La Paz, MexicoDepartment of Cell Biology, Physiology, and Immunology, University of Barcelona, Barcelona, SpainAquaculture Program, Institute of Agrifood Research and Technology (IRTA), La Ràpita, SpainThe present study explores the effects of two supplementation levels of Debaryomyces hansenii (1.1% and 2.2%) as a probiotic in a reference low fish meal-based diet on the skin mucosal tissue in Sparus aurata. This study includes the evaluation of fish performance coupled with a holistic study of the skin mucosa: i) a transcriptomic study of the skin tissue, and ii) the evaluation of its secreted mucus both in terms of skin mucosal-associated biomarkers and its defensive capacity by means of co-culture analysis with two pathogenic bacteria. Results showed that after 70 days of diet administration, fish fed the diet supplemented with D. hansenii at 1.1% presented increased somatic growth and a better feed conversion ratio, compared to fish fed the control diet. In contrast, fish fed the diet including 2.2% of the probiotic presented intermediate values. Regarding gene regulation, the probiotic administration at 1.1% resulted in 712 differentially expressed genes (DEGs), among which 53.4% and 46.6% were up- and down-regulated, respectively. In particular, D. hansenii modulated some skin biological processes related to immunity and metabolism. Specifically, D. hansenii administration induced a strong modulation of some immune biological-related processes (61 DEGs), mainly involved in B- and T-cell regulatory pathways. Furthermore, dietary D. hansenii promoted the skin barrier function by the upregulation of anchoring junction genes (23 DEGs), which reinforces the physical defense against potential skin damage. In contrast, the skin showed modulated genes related to extracellular exosome and membrane organization (50 DEGs). This modulated functioning is of great interest, particularly in relation to the increased skin mucus defensive capacity observed in the bacterial co-culture in vitro trials, which could be related to the increased modulation and exudation of the innate immune components from the skin cells into the mucus. In summary, the modulation of innate immune parameters coupled with increased skin barrier function and cell trafficking potentiates the skin’s physical barrier and mucus defensive capacity, while maintaining the skin mucosa’s homeostatic immune and metabolic status. These findings confirmed the advantages of D. hansenii supplementation in low fish meal-based diets, demonstrating the probiotic benefits on cultured marine species.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1247199/fullDebaryomyces hanseniiskin defenseskin mucus defenseskin mucus associated biomarkerstranscriptomicsyeast probiotic
spellingShingle Ignasi Sanahuja
Laura Fernandez-Alacid
Silvia Torrecillas
Alberto Ruiz
Eva Vallejos-Vidal
Joana P. Firmino
Felipe E. Reyes-Lopez
Lluis Tort
Dariel Tovar-Ramirez
Antoni Ibarz
Enric Gisbert
Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
Frontiers in Immunology
Debaryomyces hansenii
skin defense
skin mucus defense
skin mucus associated biomarkers
transcriptomics
yeast probiotic
title Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
title_full Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
title_fullStr Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
title_full_unstemmed Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
title_short Dietary Debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
title_sort dietary debaryomyces hansenii promotes skin and skin mucus defensive capacities in a marine fish model
topic Debaryomyces hansenii
skin defense
skin mucus defense
skin mucus associated biomarkers
transcriptomics
yeast probiotic
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1247199/full
work_keys_str_mv AT ignasisanahuja dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT laurafernandezalacid dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT silviatorrecillas dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT albertoruiz dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT evavallejosvidal dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT joanapfirmino dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT felipeereyeslopez dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT lluistort dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT darieltovarramirez dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT antoniibarz dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel
AT enricgisbert dietarydebaryomyceshanseniipromotesskinandskinmucusdefensivecapacitiesinamarinefishmodel