Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)

Gut microbial communities are highly dynamic and respond to factors such as diet and host metabolism. However, there is limited knowledge on changes in gut microbiota during the daily cycle. To investigate how interactions between feeding and water temperature affected the diurnal dynamics and activ...

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Main Authors: Carmen Navarro-Guillén, Eirik Degré Lorentsen, Erick Perera, Manuel Yúfera, Olav Vadstein
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2023.1236305/full
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author Carmen Navarro-Guillén
Eirik Degré Lorentsen
Erick Perera
Manuel Yúfera
Olav Vadstein
author_facet Carmen Navarro-Guillén
Eirik Degré Lorentsen
Erick Perera
Manuel Yúfera
Olav Vadstein
author_sort Carmen Navarro-Guillén
collection DOAJ
description Gut microbial communities are highly dynamic and respond to factors such as diet and host metabolism. However, there is limited knowledge on changes in gut microbiota during the daily cycle. To investigate how interactions between feeding and water temperature affected the diurnal dynamics and activity of the microbiota, we analyzed the qualitative and quantitative composition in feces of the potentially active bacterial community along a day cycle in greater amberjack juveniles (Seriola dumerili). Bacterial density (based on qPCR of 16S rDNA) in feces was relatively stable along the day. In contrast bacterial activity (based on qPCR of 16S rRNA) increased during the period of active feeding, and was reduced to pre-feeding levels four hours after the last meal. The relative potential activity of the bacterial community in fish feces varied with postprandial time. At the phylum level there was a shift from a Spirochaetes-dominated community in the morning to increased potential activity of Proteobacteria after feeding. At lower taxonomic level, i.e. order, the bacterial community was dominated by Mycoplasmoidales, which relative potential activity was maintained throughout the day in all treatments. By contrast, for absolute potential bacterial activity at the order level there was a peak in potential activity of several bacterial orders at 6h after first feeding, with the most noticeable increase observed for Mycoplasmoidales. Results from the present work also indicated a close relation between the effect of water temperature and microbial dynamics. This is the first study assessing the quantitative and qualitative effects of water temperature and daily feeding rhythm on the gut microbiota dynamics in fish. Feeding was the main driver modulating bacterial activity, promoting a peak in bacterial activity 6h after first feeding. However, water temperature also modulated gut microbiota dynamics, with a marked effect on the time scale. In addition, results indicate that analysis of absolute bacterial potential activity provides a better resolution of metabolically active gut microbial community, since a change in the absolute activity of a single taxon can alter the relative activity of all taxa.
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spelling doaj.art-eb2b73103fb643c0b59340870d6faa0a2023-09-13T05:26:39ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-09-011010.3389/fmars.2023.12363051236305Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)Carmen Navarro-Guillén0Eirik Degré Lorentsen1Erick Perera2Manuel Yúfera3Olav Vadstein4Departamento de Biología Marina y Acuicultura. Instituto de Ciencias Marinas de Andalucía (ICMAN-CSIC), Puerto Real, SpainDepartment of Biotechnology and Food Science, Norwegian University of Science and Technology (NTNU), Trondheim, NorwayDepartamento de Biología Marina y Acuicultura. Instituto de Ciencias Marinas de Andalucía (ICMAN-CSIC), Puerto Real, SpainDepartamento de Biología Marina y Acuicultura. Instituto de Ciencias Marinas de Andalucía (ICMAN-CSIC), Puerto Real, SpainDepartment of Biotechnology and Food Science, Norwegian University of Science and Technology (NTNU), Trondheim, NorwayGut microbial communities are highly dynamic and respond to factors such as diet and host metabolism. However, there is limited knowledge on changes in gut microbiota during the daily cycle. To investigate how interactions between feeding and water temperature affected the diurnal dynamics and activity of the microbiota, we analyzed the qualitative and quantitative composition in feces of the potentially active bacterial community along a day cycle in greater amberjack juveniles (Seriola dumerili). Bacterial density (based on qPCR of 16S rDNA) in feces was relatively stable along the day. In contrast bacterial activity (based on qPCR of 16S rRNA) increased during the period of active feeding, and was reduced to pre-feeding levels four hours after the last meal. The relative potential activity of the bacterial community in fish feces varied with postprandial time. At the phylum level there was a shift from a Spirochaetes-dominated community in the morning to increased potential activity of Proteobacteria after feeding. At lower taxonomic level, i.e. order, the bacterial community was dominated by Mycoplasmoidales, which relative potential activity was maintained throughout the day in all treatments. By contrast, for absolute potential bacterial activity at the order level there was a peak in potential activity of several bacterial orders at 6h after first feeding, with the most noticeable increase observed for Mycoplasmoidales. Results from the present work also indicated a close relation between the effect of water temperature and microbial dynamics. This is the first study assessing the quantitative and qualitative effects of water temperature and daily feeding rhythm on the gut microbiota dynamics in fish. Feeding was the main driver modulating bacterial activity, promoting a peak in bacterial activity 6h after first feeding. However, water temperature also modulated gut microbiota dynamics, with a marked effect on the time scale. In addition, results indicate that analysis of absolute bacterial potential activity provides a better resolution of metabolically active gut microbial community, since a change in the absolute activity of a single taxon can alter the relative activity of all taxa.https://www.frontiersin.org/articles/10.3389/fmars.2023.1236305/fullbacteria potential activitydiel oscillationsfeedingfish physiologygut microbiotaquantitative bacteria composition
spellingShingle Carmen Navarro-Guillén
Eirik Degré Lorentsen
Erick Perera
Manuel Yúfera
Olav Vadstein
Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
Frontiers in Marine Science
bacteria potential activity
diel oscillations
feeding
fish physiology
gut microbiota
quantitative bacteria composition
title Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
title_full Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
title_fullStr Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
title_full_unstemmed Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
title_short Feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles (Seriola dumerili)
title_sort feeding and water temperature modulate the potential activity of gut microbiota in greater amberjack juveniles seriola dumerili
topic bacteria potential activity
diel oscillations
feeding
fish physiology
gut microbiota
quantitative bacteria composition
url https://www.frontiersin.org/articles/10.3389/fmars.2023.1236305/full
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