Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout

Abstract Background Recirculating aquaculture systems can cause chronic stress in fish when stocking density is too high. However, this study tested whether low stocking density can cause fish stress. Adult rainbow trout, with an average weight of 1.517 kg (± 0.39), were subjected to low (12 kg/m3 ±...

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Main Authors: Guglielmo Raymo, Fabiane Januario, Ali Ali, Ridwan O. Ahmed, Rafet Al-Tobasei, Mohamed Salem
Format: Article
Language:English
Published: BMC 2024-10-01
Series:Animal Microbiome
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Online Access:https://doi.org/10.1186/s42523-024-00344-1
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author Guglielmo Raymo
Fabiane Januario
Ali Ali
Ridwan O. Ahmed
Rafet Al-Tobasei
Mohamed Salem
author_facet Guglielmo Raymo
Fabiane Januario
Ali Ali
Ridwan O. Ahmed
Rafet Al-Tobasei
Mohamed Salem
author_sort Guglielmo Raymo
collection DOAJ
description Abstract Background Recirculating aquaculture systems can cause chronic stress in fish when stocking density is too high. However, this study tested whether low stocking density can cause fish stress. Adult rainbow trout, with an average weight of 1.517 kg (± 0.39), were subjected to low (12 kg/m3 ± 0.94) and moderate (43 kg/m3 ± 2.03) stocking densities for 24 days in a recirculating system maintained at 15 °C. At the end of the experiment, fecal microbiome analysis was carried out using a 16S rRNA amplicon sequencing. Additionally, an untargeted plasma metabolomics analysis was conducted. Results The moderate stocking density group harboured greater numbers of commensals, such as C. somerae, R. lituseburensis, and L. plantarum. In contrast, detrimental species such as S. putrifacens and P. putida were abundant in the low-stocking density fish. Functional microbiome profiling revealed vitamin B12 salvage and synthesis in moderate stocking densities, which may support intestinal tight junction function. Additionally, vitamin B1 biosynthesis pathways were more abundant in the moderate stocking density group, which may function towards oxidative energy metabolism and protect against oxidative stress. A complementary plasma metabolomics study, although done at slightly different stocking densities and duration, confirmed the presence of blood metabolic stress markers. Elevated levels of L-lactic acid and L-Norvaline, L-Valine, and L-glutamine, indicate low stocking density fish were under stress. Furthermore, a P4HA2 stress gene biomarker confirmed the occurrence of stress in low-density fish. This study suggests that low stocking density can induce stress in fish. Moreover, moderate stocking density leads to a distinct and beneficial fecal microbiome profile. Conclusion Our study highlights the potential benefits of optimizing the stocking density of fish in recirculating aquaculture systems. This can improve fish health and welfare, promoting a more resilient fecal microbiome. Graphical abstract
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spelling doaj-art-b94d9a835de844729668cdc1f3ac63222025-08-20T02:17:53ZengBMCAnimal Microbiome2524-46712024-10-016111210.1186/s42523-024-00344-1Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow troutGuglielmo Raymo0Fabiane Januario1Ali Ali2Ridwan O. Ahmed3Rafet Al-Tobasei4Mohamed Salem5Department of Animal and Avian Sciences, University of MarylandDepartment of Animal and Avian Sciences, University of MarylandDepartment of Animal and Avian Sciences, University of MarylandDepartment of Animal and Avian Sciences, University of MarylandComputational Science Program, Middle Tennessee State UniversityDepartment of Animal and Avian Sciences, University of MarylandAbstract Background Recirculating aquaculture systems can cause chronic stress in fish when stocking density is too high. However, this study tested whether low stocking density can cause fish stress. Adult rainbow trout, with an average weight of 1.517 kg (± 0.39), were subjected to low (12 kg/m3 ± 0.94) and moderate (43 kg/m3 ± 2.03) stocking densities for 24 days in a recirculating system maintained at 15 °C. At the end of the experiment, fecal microbiome analysis was carried out using a 16S rRNA amplicon sequencing. Additionally, an untargeted plasma metabolomics analysis was conducted. Results The moderate stocking density group harboured greater numbers of commensals, such as C. somerae, R. lituseburensis, and L. plantarum. In contrast, detrimental species such as S. putrifacens and P. putida were abundant in the low-stocking density fish. Functional microbiome profiling revealed vitamin B12 salvage and synthesis in moderate stocking densities, which may support intestinal tight junction function. Additionally, vitamin B1 biosynthesis pathways were more abundant in the moderate stocking density group, which may function towards oxidative energy metabolism and protect against oxidative stress. A complementary plasma metabolomics study, although done at slightly different stocking densities and duration, confirmed the presence of blood metabolic stress markers. Elevated levels of L-lactic acid and L-Norvaline, L-Valine, and L-glutamine, indicate low stocking density fish were under stress. Furthermore, a P4HA2 stress gene biomarker confirmed the occurrence of stress in low-density fish. This study suggests that low stocking density can induce stress in fish. Moreover, moderate stocking density leads to a distinct and beneficial fecal microbiome profile. Conclusion Our study highlights the potential benefits of optimizing the stocking density of fish in recirculating aquaculture systems. This can improve fish health and welfare, promoting a more resilient fecal microbiome. Graphical abstracthttps://doi.org/10.1186/s42523-024-00344-1Recirculating aquacultureStressMicrobiomeMetabolomicsRainbow troutOncorhynchus mykiss
spellingShingle Guglielmo Raymo
Fabiane Januario
Ali Ali
Ridwan O. Ahmed
Rafet Al-Tobasei
Mohamed Salem
Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
Animal Microbiome
Recirculating aquaculture
Stress
Microbiome
Metabolomics
Rainbow trout
Oncorhynchus mykiss
title Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
title_full Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
title_fullStr Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
title_full_unstemmed Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
title_short Fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
title_sort fecal microbiome analysis uncovers hidden stress effects of low stocking density on rainbow trout
topic Recirculating aquaculture
Stress
Microbiome
Metabolomics
Rainbow trout
Oncorhynchus mykiss
url https://doi.org/10.1186/s42523-024-00344-1
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