The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response

The present research tested the effects of dietary nisin-producing Lactococcus lactis on growth performance, feed utilization, intestinal morphology, transcriptional response, and microbiota in gilthead sea bream (Sparus aurata). A feeding trial was conducted with fish weighting 70–90 g. Fish were t...

Full description

Bibliographic Details
Main Authors: Federico Moroni, Fernando Naya-Català, M. Carla Piazzon, Simona Rimoldi, Josep Calduch-Giner, Alberto Giardini, Inés Martínez, Fabio Brambilla, Jaume Pérez-Sánchez, Genciana Terova
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2021.659519/full
_version_ 1818608443065368576
author Federico Moroni
Fernando Naya-Català
M. Carla Piazzon
Simona Rimoldi
Josep Calduch-Giner
Alberto Giardini
Inés Martínez
Fabio Brambilla
Jaume Pérez-Sánchez
Genciana Terova
author_facet Federico Moroni
Fernando Naya-Català
M. Carla Piazzon
Simona Rimoldi
Josep Calduch-Giner
Alberto Giardini
Inés Martínez
Fabio Brambilla
Jaume Pérez-Sánchez
Genciana Terova
author_sort Federico Moroni
collection DOAJ
description The present research tested the effects of dietary nisin-producing Lactococcus lactis on growth performance, feed utilization, intestinal morphology, transcriptional response, and microbiota in gilthead sea bream (Sparus aurata). A feeding trial was conducted with fish weighting 70–90 g. Fish were tagged with passive, integrated transponders and distributed in nine 500 L tanks with 40 fish each. Fish were fed for 12 weeks with either a control (diet A) or experimental diets (diets B and C) in triplicate (3 tanks/diet). Extruded pellets of diets B and C were supplemented with a low (2 × 109 CFU/kg) and a high (5 × 109 CFU/kg) dose of probiotic, respectively. No significant differences were found between groups for the feed conversion ratio or specific growth rates. However, the final body weight of fish fed diet C was significantly higher than the control group with intermediate values for fish fed diet B. Histological analysis conducted using a semi-quantitative scoring system showed that probiotic did not alter the morphology of the intestine and did not trigger inflammation. With regard to the transcriptomic response, a customized PCR array layout was designed to simultaneously profile a panel of 44 selected genes. Significant differences in the expression of key genes involved in innate and acquired immunity were detected between fish fed probiotic and control diets. To analyze the microbiota associated to the feeds and the gut autochthonous microbial communities, we used the Illumina MiSeq platform for sequencing the 16S rRNA gene and a metagenomics pipeline based on VSEARCH and RDP databases. The analysis of gut microbiota revealed a lack of colonization of the probiotic in the host’s intestinal mucosa. However, probiotic did modulate the fish gut microbiota, confirming that colonization is not always necessary to induce host modification. In fact, diets B and C were enriched with Actinomycetales, as compared to diet A, which instead showed a higher percentage of Pseudomonas, Sphyngomonas, and Lactobacillus genera. These results were confirmed by the clear separation of gut bacterial community of fish fed with the probiotic from the bacterial community of control fish group in the beta-diversity and PLS-DA (supervised partial least-squares discriminant analysis) analyses.
first_indexed 2024-12-16T14:42:43Z
format Article
id doaj.art-c706a73042dc4269801c62670fd03c0a
institution Directory Open Access Journal
issn 2296-7745
language English
last_indexed 2024-12-16T14:42:43Z
publishDate 2021-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Marine Science
spelling doaj.art-c706a73042dc4269801c62670fd03c0a2022-12-21T22:27:51ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452021-04-01810.3389/fmars.2021.659519659519The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional ResponseFederico Moroni0Fernando Naya-Català1M. Carla Piazzon2Simona Rimoldi3Josep Calduch-Giner4Alberto Giardini5Inés Martínez6Fabio Brambilla7Jaume Pérez-Sánchez8Genciana Terova9Department of Biotechnology and Life Sciences, University of Insubria, Varese, ItalyNutrigenomics and Fish Growth Endocrinology, Institute of Aquaculture Torre de la Sal (IATS-CSIC), Castellón, SpainFish Pathology, Institute of Aquaculture Torre de la Sal (IATS-CSIC), Castellón, SpainDepartment of Biotechnology and Life Sciences, University of Insubria, Varese, ItalyNutrigenomics and Fish Growth Endocrinology, Institute of Aquaculture Torre de la Sal (IATS-CSIC), Castellón, SpainCentro Sperimentale del Latte S.r.l., Zelo Buon Persico, ItalySacco S.r.l., Cadorago, ItalyVRM S.r.l. Naturalleva, Cologna Veneta, ItalyNutrigenomics and Fish Growth Endocrinology, Institute of Aquaculture Torre de la Sal (IATS-CSIC), Castellón, SpainDepartment of Biotechnology and Life Sciences, University of Insubria, Varese, ItalyThe present research tested the effects of dietary nisin-producing Lactococcus lactis on growth performance, feed utilization, intestinal morphology, transcriptional response, and microbiota in gilthead sea bream (Sparus aurata). A feeding trial was conducted with fish weighting 70–90 g. Fish were tagged with passive, integrated transponders and distributed in nine 500 L tanks with 40 fish each. Fish were fed for 12 weeks with either a control (diet A) or experimental diets (diets B and C) in triplicate (3 tanks/diet). Extruded pellets of diets B and C were supplemented with a low (2 × 109 CFU/kg) and a high (5 × 109 CFU/kg) dose of probiotic, respectively. No significant differences were found between groups for the feed conversion ratio or specific growth rates. However, the final body weight of fish fed diet C was significantly higher than the control group with intermediate values for fish fed diet B. Histological analysis conducted using a semi-quantitative scoring system showed that probiotic did not alter the morphology of the intestine and did not trigger inflammation. With regard to the transcriptomic response, a customized PCR array layout was designed to simultaneously profile a panel of 44 selected genes. Significant differences in the expression of key genes involved in innate and acquired immunity were detected between fish fed probiotic and control diets. To analyze the microbiota associated to the feeds and the gut autochthonous microbial communities, we used the Illumina MiSeq platform for sequencing the 16S rRNA gene and a metagenomics pipeline based on VSEARCH and RDP databases. The analysis of gut microbiota revealed a lack of colonization of the probiotic in the host’s intestinal mucosa. However, probiotic did modulate the fish gut microbiota, confirming that colonization is not always necessary to induce host modification. In fact, diets B and C were enriched with Actinomycetales, as compared to diet A, which instead showed a higher percentage of Pseudomonas, Sphyngomonas, and Lactobacillus genera. These results were confirmed by the clear separation of gut bacterial community of fish fed with the probiotic from the bacterial community of control fish group in the beta-diversity and PLS-DA (supervised partial least-squares discriminant analysis) analyses.https://www.frontiersin.org/articles/10.3389/fmars.2021.659519/fullaquaculturegilthead sea breamprobioticLactococcus lactisgut microbiotatranscriptomic
spellingShingle Federico Moroni
Fernando Naya-Català
M. Carla Piazzon
Simona Rimoldi
Josep Calduch-Giner
Alberto Giardini
Inés Martínez
Fabio Brambilla
Jaume Pérez-Sánchez
Genciana Terova
The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
Frontiers in Marine Science
aquaculture
gilthead sea bream
probiotic
Lactococcus lactis
gut microbiota
transcriptomic
title The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
title_full The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
title_fullStr The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
title_full_unstemmed The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
title_short The Effects of Nisin-Producing Lactococcus lactis Strain Used as Probiotic on Gilthead Sea Bream (Sparus aurata) Growth, Gut Microbiota, and Transcriptional Response
title_sort effects of nisin producing lactococcus lactis strain used as probiotic on gilthead sea bream sparus aurata growth gut microbiota and transcriptional response
topic aquaculture
gilthead sea bream
probiotic
Lactococcus lactis
gut microbiota
transcriptomic
url https://www.frontiersin.org/articles/10.3389/fmars.2021.659519/full
work_keys_str_mv AT federicomoroni theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT fernandonayacatala theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT mcarlapiazzon theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT simonarimoldi theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT josepcalduchginer theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT albertogiardini theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT inesmartinez theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT fabiobrambilla theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT jaumeperezsanchez theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT gencianaterova theeffectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT federicomoroni effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT fernandonayacatala effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT mcarlapiazzon effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT simonarimoldi effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT josepcalduchginer effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT albertogiardini effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT inesmartinez effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT fabiobrambilla effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT jaumeperezsanchez effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse
AT gencianaterova effectsofnisinproducinglactococcuslactisstrainusedasprobioticongiltheadseabreamsparusauratagrowthgutmicrobiotaandtranscriptionalresponse