Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle

Fish genetically selected for growth (GS) and reference (REF) fish were fed with CTRL (15% FM, 5–7% FO) or FUTURE (7.5% FM, 10% poultry meal, 2.2% poultry oil + 2.5% DHA-algae oil) diets during a 12-months production cycle. Samples from initial (t<sub>0</sub>; November 2019), intermediat...

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Main Authors: Fernando Naya-Català, M. Carla Piazzon, Silvia Torrecillas, Socorro Toxqui-Rodríguez, Josep À. Calduch-Giner, Ramón Fontanillas, Ariadna Sitjà-Bobadilla, Daniel Montero, Jaume Pérez-Sánchez
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/11/12/1744
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author Fernando Naya-Català
M. Carla Piazzon
Silvia Torrecillas
Socorro Toxqui-Rodríguez
Josep À. Calduch-Giner
Ramón Fontanillas
Ariadna Sitjà-Bobadilla
Daniel Montero
Jaume Pérez-Sánchez
author_facet Fernando Naya-Català
M. Carla Piazzon
Silvia Torrecillas
Socorro Toxqui-Rodríguez
Josep À. Calduch-Giner
Ramón Fontanillas
Ariadna Sitjà-Bobadilla
Daniel Montero
Jaume Pérez-Sánchez
author_sort Fernando Naya-Català
collection DOAJ
description Fish genetically selected for growth (GS) and reference (REF) fish were fed with CTRL (15% FM, 5–7% FO) or FUTURE (7.5% FM, 10% poultry meal, 2.2% poultry oil + 2.5% DHA-algae oil) diets during a 12-months production cycle. Samples from initial (t<sub>0</sub>; November 2019), intermediate (t<sub>1</sub>; July 2020) and final (t<sub>2</sub>; November 2020) sampling points were used for Illumina 16S rRNA gene amplicon sequencing of the adherent microbiota of anterior intestine (AI). Samples from the same individuals (t<sub>1</sub>) were also used for the gene expression profiling of AI by RNA-seq, and subsequent correlation analyses with microbiota abundances. Discriminant analyses indicated the gut bacterial succession along the production cycle with the proliferation of some valuable taxa for facing seasonality and different developmental stages. An effect of genetic background was evidenced along time, decreasing through the progression of the trial, namely the gut microbiota of GS fish was less influenced by changes in diet composition. At the same time, these fish showed wider transcriptomic landmarks in the AI to cope with these changes. Our results highlighted an enhanced intestinal sphingolipid and phospholipid metabolism, epithelial turnover and intestinal motility in GS fish, which would favour their improved performance despite the lack of association with changes in gut microbiota composition. Furthermore, in GS fish, correlation analyses supported the involvement of different taxa with the down-regulated expression of pro-inflammatory markers and the boosting of markers of extracellular remodelling and response to bacterium. Altogether, these findings support the combined action of the gut microbiome and host transcriptionally mediated effects to preserve and improve gut health and function in a scenario of different growth performance and potentiality.
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spelling doaj.art-a1c9bb472a954508a886b593c7cbd2df2023-11-24T13:22:42ZengMDPI AGBiology2079-77372022-11-011112174410.3390/biology11121744Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production CycleFernando Naya-Català0M. Carla Piazzon1Silvia Torrecillas2Socorro Toxqui-Rodríguez3Josep À. Calduch-Giner4Ramón Fontanillas5Ariadna Sitjà-Bobadilla6Daniel Montero7Jaume Pérez-Sánchez8Nutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainFish Pathology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainGrupo de Investigación en Acuicultura (GIA), IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, Crta. Taliarte s/n, 35214 Telde, Las Palmas, Canary Islands, SpainNutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainNutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainSkretting Aquaculture Research Centre, 4016 Stavanger, NorwayFish Pathology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainGrupo de Investigación en Acuicultura (GIA), IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, Crta. Taliarte s/n, 35214 Telde, Las Palmas, Canary Islands, SpainNutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la Sal (IATS, CSIC), 12595 Castellón, SpainFish genetically selected for growth (GS) and reference (REF) fish were fed with CTRL (15% FM, 5–7% FO) or FUTURE (7.5% FM, 10% poultry meal, 2.2% poultry oil + 2.5% DHA-algae oil) diets during a 12-months production cycle. Samples from initial (t<sub>0</sub>; November 2019), intermediate (t<sub>1</sub>; July 2020) and final (t<sub>2</sub>; November 2020) sampling points were used for Illumina 16S rRNA gene amplicon sequencing of the adherent microbiota of anterior intestine (AI). Samples from the same individuals (t<sub>1</sub>) were also used for the gene expression profiling of AI by RNA-seq, and subsequent correlation analyses with microbiota abundances. Discriminant analyses indicated the gut bacterial succession along the production cycle with the proliferation of some valuable taxa for facing seasonality and different developmental stages. An effect of genetic background was evidenced along time, decreasing through the progression of the trial, namely the gut microbiota of GS fish was less influenced by changes in diet composition. At the same time, these fish showed wider transcriptomic landmarks in the AI to cope with these changes. Our results highlighted an enhanced intestinal sphingolipid and phospholipid metabolism, epithelial turnover and intestinal motility in GS fish, which would favour their improved performance despite the lack of association with changes in gut microbiota composition. Furthermore, in GS fish, correlation analyses supported the involvement of different taxa with the down-regulated expression of pro-inflammatory markers and the boosting of markers of extracellular remodelling and response to bacterium. Altogether, these findings support the combined action of the gut microbiome and host transcriptionally mediated effects to preserve and improve gut health and function in a scenario of different growth performance and potentiality.https://www.mdpi.com/2079-7737/11/12/1744sea breamselective breedingnutritiongut microbiotahost transcriptomicsintestinal motility
spellingShingle Fernando Naya-Català
M. Carla Piazzon
Silvia Torrecillas
Socorro Toxqui-Rodríguez
Josep À. Calduch-Giner
Ramón Fontanillas
Ariadna Sitjà-Bobadilla
Daniel Montero
Jaume Pérez-Sánchez
Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
Biology
sea bream
selective breeding
nutrition
gut microbiota
host transcriptomics
intestinal motility
title Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
title_full Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
title_fullStr Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
title_full_unstemmed Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
title_short Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (<i>Sparus aurata</i>) Production Cycle
title_sort genetics and nutrition drive the gut microbiota succession and host transcriptome interactions through the gilthead sea bream i sparus aurata i production cycle
topic sea bream
selective breeding
nutrition
gut microbiota
host transcriptomics
intestinal motility
url https://www.mdpi.com/2079-7737/11/12/1744
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